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BioMed Research International
Volume 2015 (2015), Article ID 781087, 10 pages
http://dx.doi.org/10.1155/2015/781087
Review Article

Physiological Impact of Abnormal Lipoxin A4 Production on Cystic Fibrosis Airway Epithelium and Therapeutic Potential

1National Children’s Research Centre, Crumlin, Dublin 12, Ireland
2Royal College of Surgeons in Ireland, Beaumont Hospital, Dublin 9, Ireland
3Institut National de la Santé et de la Recherche Médicale, U845, Faculté de Médecine Paris Descartes, Site Necker, 156 rue Vaugirard, 75015 Paris, France

Received 20 June 2014; Revised 22 September 2014; Accepted 23 September 2014

Academic Editor: Carlos Artério Sorgi

Copyright © 2015 Gerard Higgins et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. D. Levy, C. B. Clish, B. Schmidt, K. Gronert, and C. N. Serhan, “Lipid mediator class switching during acute inflammation: signals in resolution,” Nature Immunology, vol. 2, no. 7, pp. 612–619, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. F. C. Ringholz, P. J. Buchanan, D. T. Clarke et al., “Reduced 15-lipoxygenase 2 and lipoxin A4/leukotriene B4 ratio in children with cystic fibrosis,” The European Respiratory Journal, vol. 44, no. 2, pp. 394–404, 2014. View at Publisher · View at Google Scholar
  3. J. Z. Haeggström and C. D. Funk, “Lipoxygenase and leukotriene pathways: biochemistry, biology, and roles in disease,” Chemical Reviews, vol. 111, no. 10, pp. 5866–5896, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. N. Mukaida, S. Okamoto, Y. Ishikawa, and K. Matsushima, “Molecular mechanism of interleukin-8 gene expression,” Journal of Leukocyte Biology, vol. 56, no. 5, pp. 554–558, 1994. View at Google Scholar · View at Scopus
  5. C. N. Serhan, S. Yacoubian, and R. Yang, “Anti-inflammatory and proresolving lipid mediators,” Annual Review of Pathology, vol. 3, pp. 279–312, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. I. M. Fierro and C. N. Serhan, “Mechanisms in anti-inflammation and resolution: the role of lipoxins and aspirin-triggered lipoxins,” Brazilian Journal of Medical and Biological Research, vol. 34, no. 5, pp. 555–566, 2001. View at Google Scholar · View at Scopus
  7. C. Chavis, I. Vachier, P. Chanez, J. Bousquet, and P. Godard, “5(S), 15(S)-dihydroxyeicosatetraenoic acid and lipoxin generation in human polymorphonuclear cells: dual specificity of 5-lipoxygenase towards endogenous and exogenous precursors,” Journal of Experimental Medicine, vol. 183, no. 4, pp. 1633–1643, 1996. View at Publisher · View at Google Scholar · View at Scopus
  8. C. N. Serhan, U. Hirsch, J. Palmblad, and B. Samuelsson, “Formation of lipoxin A by granulocytes from eosinophilic donors,” FEBS Letters, vol. 217, no. 2, pp. 242–246, 1987. View at Publisher · View at Google Scholar · View at Scopus
  9. B. D. Levy, S. Bertram, H. H. Tai et al., “Agonist-induced lipoxin A4 generation: detection by a novel lipoxin A4-ELISA,” Lipids, vol. 28, no. 12, pp. 1047–1053, 1993. View at Publisher · View at Google Scholar · View at Scopus
  10. C. N. Serhan and K.-A. Sheppard, “Lipoxin formation during human neutrophil-platelet interactions: evidence for the transformation of leukotriene A4 by platelet 12-lipoxygenase in vitro,” Journal of Clinical Investigation, vol. 85, no. 3, pp. 772–780, 1990. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Clària, M. H. Lee, and C. N. Serhan, “Aspirin-triggered lipoxins (15-epi-LX) are generated by the human lung adenocarcinoma cell line (A549)-neutrophil interactions and are potent inhibitors of cell proliferation,” Molecular Medicine, vol. 2, no. 5, pp. 583–596, 1996. View at Google Scholar · View at Scopus
  12. “Special issue: the lipoxins and the aspirin-triggered lipoxins,” Prostaglandins, Leukotrienes & Essential Fatty Acids, vol. 73, no. 3-4, pp. 139–321, 2005.
  13. B. D. Levy, M. Romano, H. A. Chapman, J. J. Reilly, J. Drazen, and C. N. Serhan, “Human alveolar macrophages have 15-lipoxygenase and generate 15(S)-hydroxy-5,8,11-cis-13-trans-eicosatetraenoic acid and lipoxins,” Journal of Clinical Investigation, vol. 92, no. 3, pp. 1572–1579, 1993. View at Publisher · View at Google Scholar · View at Scopus
  14. I. Vachier, P. Chanez, C. Bonnans, P. Godard, J. Bousquet, and C. Chavis, “Endogenous anti-inflammatory mediators from arachidonate in human neutrophils,” Biochemical and Biophysical Research Communications, vol. 290, no. 1, pp. 219–224, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. N. Chiang, M. Arita, and C. N. Serhan, “Anti-inflammatory circuitry: lipoxin, aspirin-triggered lipoxins and their receptor ALX,” Prostaglandins, Leukotrienes & Essential Fatty Acids, vol. 73, no. 3-4, pp. 163–177, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. N. Chiang, S. Hurwitz, P. M. Ridker, and C. N. Serhan, “Aspirin has a gender-dependent impact on antiinflammatory 15-epi-lipoxin A4 formation: a randomized human trial,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 26, no. 2, pp. e14–e17, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. G. Ying, P. Iribarren, Y. Zhou et al., “Humanin, a newly identified neuroprotective factor, uses the G protein-coupled formylpeptide receptor-like-1 as a functional receptor,” Journal of Immunology, vol. 172, no. 11, pp. 7078–7085, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. F. Cattaneo, M. Parisi, and R. Ammendola, “Distinct signaling cascades elicited by different formyl peptide receptor 2 (FPR2) agonists,” International Journal of Molecular Sciences, vol. 14, no. 4, pp. 7193–7230, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. R. D. Ye, F. Boulay, M. W. Ji et al., “International union of basic and clinical pharmacology. Lxxiii. Nomenclature for the formyl peptide receptor (fpr) family,” Pharmacological Reviews, vol. 61, no. 2, pp. 119–161, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. N. Chiang, C. N. Serhan, S.-E. Dahlén et al., “The lipoxin receptor ALX: potent ligand-specific and stereoselective actions in vivo,” Pharmacological Reviews, vol. 58, no. 3, pp. 463–487, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. C. N. Serhan, “Lipoxins and aspirin-triggered 15-epi-lipoxin biosynthesis: an update and role in anti-inflammation and pro-resolution,” Prostaglandins and Other Lipid Mediators, vol. 68-69, pp. 433–455, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Bonnans, K. Fukunaga, M. A. Levy, and B. D. Levy, “Lipoxin A4 regulates bronchial epithelial cell responses to acid injury,” The American Journal of Pathology, vol. 168, no. 4, pp. 1064–1072, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. S. P. Colgan, C. N. Serhan, C. A. Parkos, C. Delp-Archer, and J. L. Madara, “Lipoxin A4 modulates transmigration of human neutrophils across intestinal epithelial monolayers,” Journal of Clinical Investigation, vol. 92, no. 1, pp. 75–82, 1993. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Takano, C. B. Clish, K. Gronert, N. Petasis, and C. N. Serhan, “Neutrophil-mediated changes in vascular permeability are inhibited by topical application of aspirin-triggered 15-epi-lipoxin A4 and novel lipoxin B4 stable analogues,” The Journal of Clinical Investigation, vol. 101, no. 4, pp. 819–826, 1998. View at Publisher · View at Google Scholar · View at Scopus
  25. L. József, C. Zouki, N. A. Petasis, C. N. Serhan, and J. G. Filep, “Lipoxin A4 and aspirin-triggered 15-epi-lipoxin A4 inhibit peroxynitrite formation, NF-κB and AP-1 activation, and IL-8 gene expression in human leukocytes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 20, pp. 13266–13271, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Bonnans and B. D. Levy, “Lipid mediators as agonists for the resolution of acute lung inflammation and injury,” The American Journal of Respiratory Cell and Molecular Biology, vol. 36, no. 2, pp. 201–205, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. A. T. Gewirtz, B. McCormick, A. S. Neish et al., “Pathogen-induced chemokine secretion for model intestinal epithelium is inhibited by lipoxin A4 analogs,” Journal of Clinical Investigation, vol. 101, no. 9, pp. 1860–1869, 1998. View at Publisher · View at Google Scholar · View at Scopus
  28. V. Verriere, Y. Grumbach, R. Chiron, and V. Urbach, “LXA4 effect on intracellular Ca2+, Cl secretion and IL-8 production in normal and CF airway epithelium,” Revue des Maladies Respiratoires, vol. 23, no. 5, p. 574, 2006. View at Google Scholar
  29. C. L. Karp, L. M. Flick, K. W. Park et al., “Defective lipoxin-mediated anti-inflammatory activity in the cystic fibrosis airway,” Nature Immunology, vol. 5, no. 4, pp. 388–392, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Godson, S. Mitchell, K. Harvey, N. A. Petasis, N. Hogg, and H. R. Brady, “Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages,” Journal of Immunology, vol. 164, no. 4, pp. 1663–1667, 2000. View at Publisher · View at Google Scholar · View at Scopus
  31. B. McMahon, S. Mitchell, H. R. Brady, and C. Godson, “Lipoxins: revelations on resolution,” Trends in Pharmacological Sciences, vol. 22, no. 8, pp. 391–395, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. D. H. Andersen, “Cystic fibrosis of the pancreas and its relation to celiac disease: a clinical and pathologic study,” Archives of Pediatrics & Adolescent Medicine, vol. 56, no. 2, pp. 344–399, 1938. View at Publisher · View at Google Scholar
  33. L.-C. Tsui, M. Buchwald, D. Barker et al., “Cystic fibrosis locus defined by a genetically linked polymorphic DNA marker,” Science, vol. 230, no. 4729, pp. 1054–1057, 1985. View at Publisher · View at Google Scholar · View at Scopus
  34. B. J. Wainwright, P. J. Scambler, J. Schmidtke et al., “Localization of cystic fibrosis locus to human chromosome 7cen-q22,” Nature, vol. 318, no. 6044, pp. 384–385, 1985. View at Publisher · View at Google Scholar · View at Scopus
  35. R. White, S. Woodward, M. Leppert et al., “A closely linked genetic marker for cystic fibrosis,” Nature, vol. 318, no. 6044, pp. 382–384, 1985. View at Publisher · View at Google Scholar · View at Scopus
  36. J. R. Riordan, J. M. Rommens, B.-S. Kerem et al., “Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA,” Science, vol. 245, no. 4922, pp. 1066–1073, 1989. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Bush, E. Alton, J. C. Davies, U. Griesenbach, and A. Jaffe, Eds., Cystic Fibrosis in the 21st Century: Progress in Respiratory Research, Karger, Basel, Switzerland, 2006.
  38. M. Wilschanski, J. Zielenski, D. Markiewicz et al., “Correlation of sweat chloride concentration with classes of the cystic fibrosis transmembrane conductance regulator gene mutations,” The Journal of Pediatrics, vol. 127, no. 5, pp. 705–710, 1995. View at Publisher · View at Google Scholar · View at Scopus
  39. M. J. Welsh and A. E. Smith, “Molecular mechanisms of CFTR chloride channel dysfunction in cystic fibrosis,” Cell, vol. 73, no. 7, pp. 1251–1254, 1993. View at Publisher · View at Google Scholar · View at Scopus
  40. J. F. Engelhardt, J. R. Yankaskas, S. A. Ernst et al., “Submucosal glands are the predominant site of CFTR expression in the human bronchus,” Nature genetics, vol. 2, no. 3, pp. 240–248, 1992. View at Publisher · View at Google Scholar · View at Scopus
  41. A. E. O. Trezise and M. Buchwald, “In vivo cell-specific expression of the cystic fibrosis transmembrane conductance regulator,” Nature, vol. 353, no. 6343, pp. 434–437, 1991. View at Publisher · View at Google Scholar · View at Scopus
  42. N. Kartner, O. Augustinas, T. J. Jensen, A. L. Naismith, and J. R. Riordan, “Mislocalization of ΔF508 CFTR in cystic fibrosis sweat gland,” Nature Genetics, vol. 1, no. 5, pp. 321–327, 1992. View at Publisher · View at Google Scholar · View at Scopus
  43. A. E. Trezise, J. A. Chambers, C. J. Wardle, S. Gould, and A. Harris, “Expression of the cystic fibrosis gene in human foetal tissues,” Human Molecular Genetics, vol. 2, no. 3, pp. 213–218, 1993. View at Publisher · View at Google Scholar · View at Scopus
  44. A. L. Manson, A. E. O. Trezise, L. J. MacVinish et al., “Complementation of null CF mice with a human CFTR YAC transgene,” The EMBO Journal, vol. 16, no. 14, pp. 4238–4249, 1997. View at Publisher · View at Google Scholar · View at Scopus
  45. T. F. Boat and P. W. Cheng, “Epithelial cell dysfunction in cystic fibrosis: implications for airways disease,” Acta Paediatrica Scandinavica, Supplement, vol. 363, pp. 25–29, 1989. View at Google Scholar · View at Scopus
  46. J. E. Mickle, M. Macek Jr., S. B. Fulmer-Smentek et al., “A mutation in the cystic fibrosis transmembrane conductance regulator gene associated with elevated sweat chloride concentrations in the absence of cystic fibrosis,” Human Molecular Genetics, vol. 7, no. 4, pp. 729–735, 1998. View at Publisher · View at Google Scholar · View at Scopus
  47. R. G. Painter, V. G. Valentine, N. A. Lanson Jr. et al., “CFTR expression in human neutrophils and the phagolysosomal chlorination defect in cystic fibrosis,” Biochemistry, vol. 45, no. 34, pp. 10260–10269, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. R. G. Painter, R. W. Bonvillain, V. G. Valentine et al., “The role of chloride anion and CFTR in killing of Pseudomonas aeruginosa by normal and CF neutrophils,” Journal of Leukocyte Biology, vol. 83, no. 6, pp. 1345–1353, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Di, M. E. Brown, L. V. Deriy et al., “CFTR regulates phagosome acidification in macrophages and alters bactericidal activity,” Nature Cell Biology, vol. 8, no. 9, pp. 933–944, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. T. L. Bonfield, C. A. Hodges, C. U. Cotton, and M. L. Drumm, “Absence of the cystic fibrosis transmembrane regulator (Cftr) from myeloid-derived cells slows resolution of inflammation and infection,” Journal of Leukocyte Biology, vol. 92, no. 5, pp. 1111–1122, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. A. M. van Heeckeren and M. D. Schluchter, “Murine models of chronic Pseudomonas aeruginosa lung infection,” Laboratory Animals, vol. 36, no. 3, pp. 291–312, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Bonnans, I. Vachier, C. Chavis, P. Godard, J. Bousquet, and P. Chanez, “Lipoxins are potential endogenous antiinflammatory mediators in asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 165, no. 11, pp. 1531–1535, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Planagumà, S. Kazani, G. Marigowda et al., “Airway lipoxin A4 generation and lipoxin A4 receptor expression are decreased in severe asthma,” The American Journal of Respiratory and Critical Care Medicine, vol. 178, no. 6, pp. 574–582, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. L. Balode, G. Strazda, N. Jurka et al., “Lipoxygenase-derived arachidonic acid metabolites in chronic obstructive pulmonary disease,” Medicina, vol. 48, no. 6, pp. 292–298, 2012. View at Google Scholar · View at Scopus
  55. R. Chiron, Y. Y. Grumbach, N. V. T. Quynh, V. Verriere, and V. Urbach, “Lipoxin A4 and interleukin-8 levels in cystic fibrosis sputum after antibiotherapy,” Journal of Cystic Fibrosis, vol. 7, no. 6, pp. 463–468, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. V. Starosta, F. Ratjen, E. Rietschel, K. Paul, and M. Griese, “Anti-inflammatory cytokines in cystic fibrosis lung disease,” European Respiratory Journal, vol. 28, no. 3, pp. 581–587, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. T. Carlo, H. Kalwa, and B. D. Levy, “15-Epi-lipoxin A4 inhibits human neutrophil superoxide anion generation by regulating polyisoprenyl diphosphate phosphatase 1,” The FASEB Journal, vol. 27, no. 7, pp. 2733–2741, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. D. Mattoscio, V. Evangelista, R. De Cristofaro et al., “Cystic fibrosis transmembrane conductance regulator (CFTR) expression in human platelets: impact on mediators and mechanisms of the inflammatory response,” The FASEB Journal, vol. 24, no. 10, pp. 3970–3980, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. R. C. Boucher, “Airway surface dehydration in cystic fibrosis: pathogenesis and therapy,” Annual Review of Medicine, vol. 58, pp. 157–170, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. H. Matsui, C. W. Davis, R. Tarran, and R. C. Boucher, “Osmotic water permeabilities of cultured, well-differentiated normal and cystic fibrosis airway epithelia,” Journal of Clinical Investigation, vol. 105, no. 10, pp. 1419–1427, 2000. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Kunzelmann, G. L. Kiser, R. Schreibe, and J. R. Riordan, “Inhibition of epithelial Na+ currents by intracellular domains of the cystic fibrosis transmembrane conductance regulator,” FEBS Letters, vol. 400, no. 3, pp. 341–344, 1997. View at Publisher · View at Google Scholar · View at Scopus
  62. M. J. Stutts, C. M. Canessa, J. C. Olsen et al., “CFTR as a cAMP-Dependent regulator of sodium channels,” Science, vol. 269, no. 5225, pp. 847–850, 1995. View at Publisher · View at Google Scholar · View at Scopus
  63. P. B. Davis, M. Drumm, and M. W. Konstan, “Cystic fibrosis,” American Journal of Respiratory and Critical Care Medicine, vol. 154, no. 5, pp. 1229–1256, 1996. View at Publisher · View at Google Scholar · View at Scopus
  64. D. Worlitzsch, R. Tarran, M. Ulrich et al., “Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients,” The Journal of Clinical Investigation, vol. 109, no. 3, pp. 317–325, 2002. View at Publisher · View at Google Scholar · View at Scopus
  65. R. C. Boucher, M. J. Stutts, M. R. Knowles, L. Cantley, and J. T. Gatzy, “Na+ transport in cystic fibrosis respiratory epithelia. Abnormal basal rate and response to adenylate cyclase activation,” Journal of Clinical Investigation, vol. 78, no. 5, pp. 1245–1252, 1986. View at Publisher · View at Google Scholar · View at Scopus
  66. R. C. Boucher, “Regulation of airway surface liquid volume by human airway epithelia,” Pflügers Archiv, vol. 445, no. 4, pp. 495–498, 2003. View at Google Scholar · View at Scopus
  67. F. Antigny, C. Norez, F. Becq, and C. Vandebrouck, “CFTR and Ca2+ signaling in cystic fibrosis,” Frontiers in Pharmacology, vol. 2, no. 67, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. N. Pillarisetti, B. Linnane, and S. Ranganathan, “Early bronchiectasis in cystic fibrosis detected by surveillance CT,” Respirology, vol. 15, no. 6, pp. 1009–1011, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. N. Pillarisetti, E. Williamson, B. Linnane et al., “Infection, inflammation,and lung function decline in infants with cystic fibrosis,” The American Journal of Respiratory and Critical Care Medicine, vol. 184, no. 1, pp. 75–81, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. F. Ratjen, “What's new in CF airway inflammation: an update,” Paediatric Respiratory Reviews, vol. 7, supplement 1, pp. S70–S72, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. C. Bonnans, P. Chanez, H. Meziane, P. Godard, J. Bousquet, and I. Vachier, “Glucocorticoid receptor-binding characteristics in severe asthma,” European Respiratory Journal, vol. 21, no. 6, pp. 985–988, 2003. View at Publisher · View at Google Scholar · View at Scopus
  72. V. Verrière, G. Higgins, M. Al-Alawi et al., “Lipoxin a4 stimulates calcium-activated chloride currents and increases airway surface liquid height in normal and cystic fibrosis airway epithelia,” PLoS ONE, vol. 7, no. 5, Article ID e37746, 2012. View at Publisher · View at Google Scholar · View at Scopus
  73. M. Al-Alawi, P. Buchanan, V. Verriere et al., “Physiological levels of lipoxin a4 inhibit enac and restore airway surface liquid height in cystic fibrosis bronchial epithelium,” Physiological Reports, vol. 2, no. 8, 2014. View at Publisher · View at Google Scholar
  74. S. J. Mason, A. M. Paradiso, and R. C. Boucher, “Regulation of transepithelial ion transport and intracellular calcium by extracellular ATP in human normal and cystic fibrosis airway epithelium,” British Journal of Pharmacology, vol. 103, no. 3, pp. 1649–1656, 1991. View at Publisher · View at Google Scholar · View at Scopus
  75. M. R. Knowles, L. L. Clarke, and R. C. Boucher, “Activation by extracellular nucleotides of chloride secretion in the airway epithelia of patients with cystic fibrosis,” The New England Journal of Medicine, vol. 325, no. 8, pp. 533–538, 1991. View at Publisher · View at Google Scholar · View at Scopus
  76. E. R. Lazarowski, R. Tarran, B. R. Grubb, C. A. van Heusden, S. Okada, and R. C. Boucher, “Nucleotide release provides a mechanism for airway surface liquid homeostasis,” The Journal of Biological Chemistry, vol. 279, no. 35, pp. 36855–36864, 2004. View at Publisher · View at Google Scholar · View at Scopus
  77. B. M. Rollins, M. Burn, R. D. Coakley et al., “A2B adenosine receptors regulate the mucus clearance component of the lung's innate defense system,” The American Journal of Respiratory Cell and Molecular Biology, vol. 39, no. 2, pp. 190–197, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. M. Mall, A. Wissner, T. Gonska et al., “Inhibition of amiloride-sensitive epithelial Na+ absorption by extracellular nucleotides in human normal and cystic fibrosis airways,” The American Journal of Respiratory Cell and Molecular Biology, vol. 23, no. 6, pp. 755–761, 2000. View at Publisher · View at Google Scholar · View at Scopus
  79. E. R. Lazarowski and R. C. Boucher, “Purinergic receptors in airway epithelia,” Current Opinion in Pharmacology, vol. 9, no. 3, pp. 262–267, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. I. M. Lorenzo, W. Liedtke, M. J. Sanderson, and M. A. Valverde, “TRPV4 channel participates in receptor-operated calcium entry and ciliary beat frequency regulation in mouse airway epithelial cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 34, pp. 12611–12616, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. D. Communi, S. Pirotton, M. Parmentier, and J.-M. Boeynaems, “Cloning and functional expression of a human uridine nucleotide receptor,” Journal of Biological Chemistry, vol. 270, no. 52, pp. 30849–30852, 1995. View at Publisher · View at Google Scholar · View at Scopus
  82. K. R. Vaughan, L. Stokes, L. R. Prince et al., “Inhibition of neutrophil apoptosis by ATP is mediated by the P2Y11 receptor,” The Journal of Immunology, vol. 179, no. 12, pp. 8544–8553, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. Z. Xiao, M. Yang, Q. Lv et al., “P2Y11 impairs cell proliferation by induction of cell cycle arrest and sensitizes endothelial cells to cisplatin-induced cell death,” Journal of Cellular Biochemistry, vol. 112, no. 9, pp. 2257–2265, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. T. D. Nguyen, S. Meichle, U. S. Kim, T. Wong, and M. W. Moody, “P2Y11, a purinergic receptor acting via cAMP, mediates secretion by pancreatic duct epithelial cells,” American Journal of Physiology: Gastrointestinal and Liver Physiology, vol. 280, no. 5, pp. G795–G804, 2001. View at Google Scholar · View at Scopus
  85. R. S. Sprague, M. L. Ellsworth, A. H. Stephenson, and A. J. Lonigro, “ATP: the red blood cell link to NO and local control of the pulmonary circulation,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 271, no. 6, part 2, pp. H2717–H2722, 1996. View at Google Scholar · View at Scopus
  86. G. Dahl and S. Locovei, “Pannexin: to gap or not to gap, is that a question?” IUBMB Life, vol. 58, no. 7, pp. 409–419, 2006. View at Publisher · View at Google Scholar · View at Scopus
  87. L. Seminario-Vidal, S. Kreda, L. Jones et al., “Thrombin promotes release of ATP from lung epithelial cells through coordinated activation of Rho- and Ca2+-dependent signaling pathways,” Journal of Biological Chemistry, vol. 284, no. 31, pp. 20638–20648, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. G. A. Ransford, N. Fregien, F. Qiu, G. Dahl, G. E. Conner, and M. Salathe, “Pannexin 1 contributes to ATP release in airway epithelia,” The American Journal of Respiratory Cell and Molecular Biology, vol. 41, no. 5, pp. 525–534, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. N. Regamey, P. K. Jeffery, E. W. Alton, A. Bush, and J. C. Davies, “Airway remodelling and its relationship to inflammation in cystic fibrosis,” Thorax, vol. 66, no. 7, pp. 624–629, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. B. R. Stripp and S. D. Reynolds, “Maintenance and repair of the bronchiolar epithelium,” Proceedings of the American Thoracic Society, vol. 5, no. 3, pp. 328–333, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. J. M. Zahm, M. Chevillard, and E. Puchelle, “Wound repair of human surface respiratory epithelium,” The American Journal of Respiratory Cell and Molecular Biology, vol. 5, no. 3, pp. 242–248, 1991. View at Publisher · View at Google Scholar · View at Scopus
  92. J. M. Zahm, H. Kaplan, A. L. Hérard et al., “Cell migration and proliferation during the in vitro wound repair of the respiratory epithelium,” Cell Motility and the Cytoskeleton, vol. 37, no. 1, pp. 33–43, 1997. View at Publisher · View at Google Scholar
  93. J. S. Erjefalt, I. Erjefalt, F. Sundler, and C. G. A. Persson, “In vivo restitution of airway epithelium,” Cell and Tissue Research, vol. 281, no. 2, pp. 305–316, 1995. View at Publisher · View at Google Scholar · View at Scopus
  94. N. T. N. Trinh, O. Bardou, A. Privé et al., “Improvement of defective cystic fibrosis airway epithelial wound repair after CFTR rescue,” European Respiratory Journal, vol. 40, no. 6, pp. 1390–1400, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. E. Maillé, N. T. N. Trinh, A. Privé et al., “Regulation of normal and cystic fibrosis airway epithelial repair processes by TNF-κ after injury,” American Journal of Physiology: Lung Cellular and Molecular Physiology, vol. 301, no. 6, pp. L945–L955, 2011. View at Publisher · View at Google Scholar · View at Scopus
  96. N. T. N. Trinh, A. Privé, E. Maillé, J. Noël, and E. Brochiero, “EGF and K+ channel activity control normal and cystic fibrosis bronchial epithelia repair,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 295, no. 5, pp. L866–L880, 2008. View at Publisher · View at Google Scholar · View at Scopus
  97. N. T. N. Trinh, A. Privé, L. Kheir et al., “Involvement of KATP and KvLQT1 K+ channels in EGF-stimulated alveolar epithelial cell repair processes,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 293, no. 4, pp. L870–L882, 2007. View at Publisher · View at Google Scholar · View at Scopus
  98. R. Hajj, P. Lesimple, B. Nawrocki-Raby, P. Birembaut, E. Puchelle, and C. Coraux, “Human airway surface epithelial regeneration is delayed and abnormal in cystic fibrosis,” Journal of Pathology, vol. 211, no. 3, pp. 340–350, 2007. View at Publisher · View at Google Scholar · View at Scopus
  99. P. J. Buchanan, P. McNally, B. J. Harvey, and V. Urbach, “Lipoxin A4-mediated KATP potassium channel activation results in cystic fibrosis airway epithelial repair,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 305, no. 2, pp. L193–L201, 2013. View at Publisher · View at Google Scholar · View at Scopus
  100. P. Roger, E. Puchelle, O. Bajolet-Laudinat et al., “Fibronectin and α5β1 integrin mediate binding of Pseudomonas aeruginosa to repairing airway epithelium,” European Respiratory Journal, vol. 13, no. 6, pp. 1301–1309, 1999. View at Publisher · View at Google Scholar · View at Scopus
  101. K. Gronert, “Lipoxins in the eye and their role in wound healing,” Prostaglandins, Leukotrienes & Essential Fatty Acids, vol. 73, no. 3-4, pp. 221–229, 2005. View at Publisher · View at Google Scholar · View at Scopus
  102. S. Kenchegowda, N. G. Bazan, and H. E. P. Bazan, “EGF stimulates lipoxin A4 synthesis and modulates repair in corneal epithelial cells through ERK and p38 activation,” Investigative Ophthalmology and Visual Science, vol. 52, no. 5, pp. 2240–2249, 2011. View at Publisher · View at Google Scholar · View at Scopus
  103. S. B. Wang, K. M. Hu, K. J. Seamon, V. Mani, Y. Chen, and K. Gronert, “Estrogen negatively regulates epithelial wound healing and protective lipid mediator circuits in the cornea,” FASEB Journal, vol. 26, no. 4, pp. 1506–1516, 2012. View at Publisher · View at Google Scholar · View at Scopus
  104. K. Gronert, N. Maheshwari, N. Khan, I. R. Hassan, M. Dunn, and M. L. Schwartzman, “A role for the mouse 12/15-lipoxygenase pathway in promoting epithelial wound healing and host defense,” Journal of Biological Chemistry, vol. 280, no. 15, pp. 15267–15278, 2005. View at Publisher · View at Google Scholar · View at Scopus
  105. G. Higgins, P. Buchanan, M. Perriere et al., “Activation of P2RY11 and ATP release by lipoxin A4 restores the airway surface liquid layer and epithelial repair in cystic fibrosis,” American Journal of Respiratory Cell and Molecular Biology, vol. 51, no. 2, pp. 178–190, 2014. View at Publisher · View at Google Scholar
  106. L. Yang, D. Cranson, and V. Trinkaus-Randall, “Cellular injury induces activation of MAPK via P2Y receptors,” Journal of Cellular Biochemistry, vol. 91, no. 5, pp. 938–950, 2004. View at Publisher · View at Google Scholar · View at Scopus
  107. V. E. Klepeis, I. Weinger, E. Kaczmarek, and V. Trinkaus-Randall, “P2Y receptors play a critical role in epithelial cell communication and migration,” Journal of Cellular Biochemistry, vol. 93, no. 6, pp. 1115–1133, 2004. View at Publisher · View at Google Scholar · View at Scopus
  108. J. Yin and F.-S. X. Yu, “Erk1/2 mediate wounding- and g-protein-coupled receptor ligands-induced egfr activation via regulating adam17 and hb-egf shedding,” Investigative Ophthalmology & Visual Science, vol. 50, no. 1, pp. 132–139, 2009. View at Publisher · View at Google Scholar · View at Scopus
  109. C. L. Sherwood, R. C. Lantz, J. L. Burgess, and S. Boitano, “Arsenic alters ATP-dependent Ca2+ signaling in human airway epithelial cell wound response,” Toxicological Sciences, vol. 121, no. 1, pp. 191–206, 2011. View at Publisher · View at Google Scholar · View at Scopus
  110. T. Ko, H. J. An, Y. G. Ji, O. J. Kim, and D. H. Lee, “P2Y receptors regulate proliferation of human pancreatic duct epithelial cells,” Pancreas, vol. 41, no. 5, pp. 797–803, 2012. View at Publisher · View at Google Scholar · View at Scopus
  111. I. Boucher, C. Rich, A. Lee, M. Marcincin, and V. Trinkaus-Randall, “The P2Y2 receptor mediates the epithelial injury response and cell migration,” American Journal of Physiology—Cell Physiology, vol. 299, no. 2, pp. C411–C421, 2010. View at Publisher · View at Google Scholar · View at Scopus
  112. I. Weinger, V. E. Klepeis, and V. Trinkaus-Randall, “Tri-nucleotide receptors play a critical role in epithelial cell wound repair,” Purinergic Signalling, vol. 1, no. 3, pp. 281–292, 2005. View at Publisher · View at Google Scholar · View at Scopus
  113. É. Degagné, J. Degrandmaison, D. M. Grbic, V. Vinette, G. Arguin, and F.-P. Gendron, “P2Y2 receptor promotes intestinal microtubule stabilization and mucosal re-epithelization in experimental colitis,” Journal of Cellular Physiology, vol. 228, no. 1, pp. 99–109, 2013. View at Publisher · View at Google Scholar · View at Scopus
  114. J. N. Rao, O. Platoshyn, L. Li et al., “Activation of K+ channels and increased migration of differentiated intestinal epithelial cells after wounding,” The American Journal of Physiology—Cell Physiology, vol. 282, no. 4, pp. C885–C898, 2002. View at Publisher · View at Google Scholar · View at Scopus
  115. L. A. Pardo, “Voltage-gated potassium channels in cell proliferation,” Physiology, vol. 19, no. 5, pp. 285–292, 2004. View at Publisher · View at Google Scholar · View at Scopus
  116. W. Kessler, T. Budde, M. Gekle, A. Fabian, and A. Schwab, “Activation of cell migration with fibroblast growth factor-2 requires calcium-sensitive potassium channels,” Pflugers Archiv European Journal of Physiology, vol. 456, no. 5, pp. 813–823, 2008. View at Publisher · View at Google Scholar · View at Scopus
  117. M. M. Lotz, H. Wang, J. C. Song, S. E. Pories, and J. B. Matthews, “K+ channel inhibition accelerates intestinal epithelial cell wound healing,” Wound Repair and Regeneration, vol. 12, no. 5, pp. 565–574, 2004. View at Publisher · View at Google Scholar · View at Scopus
  118. Y. Grumbach, N. V. T. Quynh, R. Chiron, and V. Urbach, “LXA4 stimulates ZO-1 expression and transepithelial electrical resistance in human airway epithelial (16HBE14o-) cells,” American Journal of Physiology: Lung Cellular and Molecular Physiology, vol. 296, no. 1, pp. L101–L108, 2009. View at Publisher · View at Google Scholar · View at Scopus
  119. I. M. Balfour-Lynn, “Anti-inflammatory approaches to cystic fibrosis airways disease,” Current Opinion in Pulmonary Medicine, vol. 13, no. 6, pp. 522–528, 2007. View at Publisher · View at Google Scholar · View at Scopus
  120. I. M. Balfour-Lynn and K. Welch, “Inhaled corticosteroids for cystic fibrosis,” Cochrane Database of Systematic Reviews, vol. 11, 2012. View at Publisher · View at Google Scholar · View at Scopus
  121. L. C. Lands and S. Stanojevic, “Oral non-steroidal anti-inflammatory drug therapy for lung disease in cystic fibrosis,” The Cochrane Database of Systematic Reviews, vol. 6, Article ID CD001505, 2013. View at Publisher · View at Google Scholar · View at Scopus
  122. S. van Biervliet, J. P. van Biervliet, E. Robberecht, and A. Christophe, “Docosahexaenoic acid trials in cystic fibrosis: a review of the rationale behind the clinical trials,” Journal of Cystic Fibrosis, vol. 4, no. 1, pp. 27–34, 2005. View at Publisher · View at Google Scholar · View at Scopus
  123. F. J. Accurso, S. M. Rowe, J. P. Clancy et al., “Effect of VX-770 in persons with cystic fibrosis and the G551D-CFTR mutation,” The New England Journal of Medicine, vol. 363, no. 21, pp. 1991–2003, 2010. View at Publisher · View at Google Scholar · View at Scopus
  124. B. W. Ramsey, J. Davies, N. G. McElvaney et al., “A CFTR potentiator in patients with cystic fibrosis and the G551D mutation,” The New England Journal of Medicine, vol. 365, no. 18, pp. 1663–1672, 2011. View at Publisher · View at Google Scholar · View at Scopus
  125. J. P. Clancy, L. Dupont, M. W. Konstan et al., “Phase II studies of nebulised Arikace in CF patients with Pseudomonas aeruginosa infection,” Thorax, vol. 68, no. 9, pp. 818–825, 2013. View at Publisher · View at Google Scholar · View at Scopus
  126. D. K. Armstrong, S. Cunningham, J. C. Davies, and E. W. F. W. Alton, “Gene therapy in cystic fibrosis,” Archives of Disease in Childhood, vol. 99, no. 5, pp. 465–468, 2014. View at Publisher · View at Google Scholar · View at Scopus
  127. G. Pisi and A. Chetta, “Airway clearance therapy in cystic fibrosis patients,” Acta Biomedica de l'Ateneo Parmense, vol. 80, no. 2, pp. 102–106, 2009. View at Google Scholar · View at Scopus
  128. R. Tarran, B. R. Grubb, D. Parsons et al., “The CF salt controversy: in vivo observations and therapeutic approaches,” Molecular Cell, vol. 8, no. 1, pp. 149–158, 2001. View at Publisher · View at Google Scholar · View at Scopus
  129. P. E. Christie, B. W. Spur, and T. H. Lee, “The effects of lipoxin a4 on airway responses in asthmatic subjects,” The American Review of Respiratory Disease, vol. 145, no. 6, pp. 1281–1284, 1992. View at Publisher · View at Google Scholar · View at Scopus