H2O2 stimulates cystic fibrosis transmembrane conductance regulator through an autocrine prostaglandin pathway, using multidrug-resistant protein-4

American Journal of Respiratory Cell and Molecular Biology

Volumn 49, Issue 4, 2013, Pages 672-679

  Conner, Gregory E ^a   Ivonnet, Pedro ^a   Gelin, Murline ^a   Whitney, Philip ^a   Salathe, Matthias ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

CFTR; EP1; EP4; H2O2; MRP4

Indexed keywords

CYCLIC AMP; CYCLOOXYGENASE 2 INHIBITOR; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; HYDROGEN PEROXIDE; MULTIDRUG RESISTANCE PROTEIN 4; PROSTAGLANDIN E RECEPTOR 1; PROSTAGLANDIN E RECEPTOR 4; PROSTAGLANDIN SYNTHASE INHIBITOR; SHORT HAIRPIN RNA; ABCC4 PROTEIN, HUMAN; ANION; CFTR PROTEIN, HUMAN; MULTIDRUG RESISTANCE PROTEIN; PROSTAGLANDIN SYNTHASE;

APICAL MEMBRANE; ARTICLE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL STIMULATION; CONTROLLED STUDY; CYSTIC FIBROSIS; EPITHELIUM CELL; HOST RESISTANCE; HUMAN; HUMAN CELL; MUCOCILIARY CLEARANCE; NORMAL HUMAN; SIGNAL TRANSDUCTION; BRONCHUS; CELL CULTURE; CELL MEMBRANE; DRUG EFFECTS; METABOLISM; DRUG EFFECT;

ANIONS; BRONCHI; CELL MEMBRANE; CELLS, CULTURED; CYCLIC AMP; CYCLOOXYGENASE INHIBITORS; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL CELLS; HUMANS; HYDROGEN PEROXIDE; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; RECEPTORS, PROSTAGLANDIN E, EP1 SUBTYPE; RECEPTORS, PROSTAGLANDIN E, EP4 SUBTYPE;

EID: 84886564112     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0156OC     Document Type: Article

References (49)

1. Boucher RC. Cystic fibrosis: a disease of vulnerability to airway surface dehydration. Trends Mol Med 2007;13:231-240.
2. Salathe M. Regulation of mammalian ciliary beating. Annu Rev Physiol 2007;69:401-422.
3. Huang P, Gilmore E, Kultgen P, Barnes P, Milgram S, Stutts MJ. Local regulation of cystic fibrosis transmembrane regulator and epithelial sodium channel in airway epithelium. Proc Am Thorac Soc 2004;1: 33-37.
4. Schmid A, Bai G, Schmid N, Zaccolo M, Ostrowski LE, Conner GE, Fregien N, Salathe M. Real-time analysis of cAMP-mediated regulation of ciliary motility in single primary human airway epithelial cells. J Cell Sci 2006;119:4176-4186.
5. Fischer H. Mechanisms and function of Duox in epithelia of the lung. Antioxid Redox Signal 2009;11:2453-2465.
6. Moskwa P, Lorentzen D, Excoffon KJ, Zabner J, McCray PB Jr, Nauseef WM, Dupuy C, B'nfi B. A novel host defense system of airways is defective in cystic fibrosis. Am J Respir Crit Care Med 2007;175:174-183.
7. Wijkstrom-Frei C, El-Chemaly S, Ali-Rachedi R, Gerson C, Cobas MA, Forteza R, Salathe M, Conner GE. Lactoperoxidase and human airway host defense. Am J Respir Cell Mol Biol 2003;29:206-212.
8. Forteza R, Salathe M, Miot F, Forteza R, Conner GE. Regulated hydrogen peroxide production by Duox in human airway epithelial cells. Am J Respir Cell Mol Biol 2005;32:462-469.
9. Conner GE, Wijkstrom-Frei C, Randell SH, Fernandez VE, Salathe M. The lactoperoxidase system links anion transport to host defense in cystic fibrosis. FEBS Lett 2007;581:271-278.
10. Gattas MV, Forteza R, Fragoso MA, Fregien N, Salas P, SalatheM, Conner GE. Oxidative epithelial host defense is regulated by infectious and inflammatory stimuli. Free Radic Biol Med 2009;47:1450-1458.
11. Harper RW, Xu C, Eiserich JP, Chen Y, Kao CY, Thai P, Setiadi H, Wu R. Differential regulation of dual NADPH oxidases/peroxidases, Duox1 and Duox2, by Th1 and Th2 cytokines in respiratory tract epithelium. FEBS Lett 2005;579:4911-4917.
12. Harper RW, Xu C, McManus M, Heidersbach A, Eiserich JP. Duox2 exhibits potent heme peroxidase activity in human respiratory tract epithelium. FEBS Lett 2006;580:5150-5154.
13. Boots AW, Hristova M, Kasahara DI, Haenen GR, Bast A, van der Vliet A. ATP-mediated activation of the NADPH oxidase Duox1 mediates airway epithelial responses to bacterial stimuli. J Biol Chem 2009;284: 17858-17867.
14. Rada B, Leto TL. Characterization of hydrogen peroxide production by Duox in bronchial epithelial cells exposed to Pseudomonas aeruginosa. FEBS Lett 2010;584:917-922.
15. Cowley EA, Linsdell P. Oxidant stress stimulates anion secretion from the human airway epithelial cell line Calu-3: implications for cystic fibrosis lung disease. J Physiol 2002;543:201-209.
16. Ohashi T, Ito Y, Matsuno T, Sato S, Shimokata K, Kume H. Paradoxical effects of hydrogen peroxide on human airway anion secretion. J Pharmacol Exp Ther 2006;318:296-303.
17. Mall M, Wissner A, Schreiber R, Kuehr J, Seydewitz HH, Brandis M, Greger R, Kunzelmann K. Role of K(V)LQT1 in cyclic adenosine monophosphate-mediated Cl(2) secretion in human airway epithelia. Am J Respir Cell Mol Biol 2000;23:283-289.
18. Cowley EA, Linsdell P. Characterization of basolateral K1 channels underlying anion secretion in the human airway cell line Calu-3. J Physiol 2002;538:747-757.
19. Joy AP, Cowley EA. 8-iso-PGE2 stimulates anion efflux from airway epithelial cells via the EP4 prostanoid receptor. Am J Respir Cell Mol Biol 2008;38:143-152.
20. Seto V, Hirota C, Hirota S, Janssen LJ. E-ring isoprostanes stimulate a Cl conductance in airway epithelium via prostaglandin E2-selective prostanoid receptors. Am J Respir Cell Mol Biol 2008;38:88-94.
21. Bernacki SH, Nelson AL, Abdullah L, Sheehan JK, Harris A, Davis CW, Randell SH. Mucin gene expression during differentiation of human airway epithelia in vitro: Muc4 and Muc5B are strongly induced. Am J Respir Cell Mol Biol 1999;20:595-604.
22. Nlend MC, Bookman RJ, Conner GE, Salathe M. Regulator of G-protein signaling protein 2 modulates purinergic calcium and ciliary beat frequency responses in airway epithelia. Am J Respir Cell Mol Biol 2002;27:436-445.
23. Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, Davis CW, Boucher RC. Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 1998;95:1005-1015.
24. Harvey PR, Tarran R, Garoff S, Myerburg MM. Measurement of the airway surface liquid volume with simple light refraction microscopy. Am J Respir Cell Mol Biol 2011;45:592-599.
25. Dazy AC, Auger F, Bailbe D, Blouquit S, Lombet A, Marano F. The toxicity of H2O2 on the ionic homeostasis of airway epithelial cells in vitro. Toxicol In Vitro 2003;17:575-580.
26. Pezzulo AA, Starner TD, Scheetz TE, Traver GL, Tilley AE, Harvey BG, Crystal RG, McCray PB Jr, Zabner J. The air-liquid interface and use of primary cell cultures are important to recapitulate the transcriptional profile of in vivo airway epithelia. Am J Physiol Lung Cell Mol Physiol 2011;300:L25-L31.
27. Hemler ME, Cook HW, Lands WE. Prostaglandin biosynthesis can be triggered by lipid peroxides. Arch Biochem Biophys 1979;193:340-345.
28. Brenneis C, Maier TJ, Schmidt R, Hofacker A, Zulauf L, Jakobsson PJ, Scholich K, Geisslinger G. Inhibition of prostaglandin E2 synthesis by SC-560 is independent of cyclooxygenase 1 inhibition. FASEB J 2006; 20:1352-1360.
29. Jones CL, Li T, Cowley EA. The prostaglandin E2 Type 4 receptor participates in the response to acute oxidant stress in airway epithelial cells. J Pharmacol Exp Ther 2012;341:552-563.
30. Lawrence RA, Jones RL, Wilson NH. Characterization of receptors involved in the direct and indirect actions of prostaglandins E and I on the guinea-pig ileum. Br J Pharmacol 1992;105:271-278.
31. Perreira M, Jiang JK, Klutz AM, Gao ZG, Shainberg A, Lu C, Thomas CJ, Jacobson KA. 'Reversine' and its 2-substituted adenine derivatives as potent and selective A3 adenosine receptor antagonists.J MedChem 2005;48:4910-4918.
32. Clarke DL, Belvisi MG, Smith SJ, Hardaker E, Yacoub MH, Meja KK, Newton R, Slater DM, Giembycz MA. Prostanoid receptor expression by human airway smooth muscle cells and regulation of the secretion of granulocyte colony-stimulating factor. Am J Physiol Lung Cell Mol Physiol 2005;288:L238-L250.
33. Matlhagela K, Taub M. Involvement of EP1 and EP2 receptors in the regulation of the Na,K-ATPase by prostaglandins in MDCK cells. Prostaglandins Other Lipid Mediat 2006;79:101-113.
34. Rutkai I, Feher A, Erdei N, Henrion D, Papp Z, Edes I, Koller A, Kaley G, Bagi Z. Activation of prostaglandin E2 EP1 receptor increases arteriolar tone and blood pressure in mice with Type 2 diabetes. Cardiovasc Res 2009;83:148-154.
35. Tang CH, Yang RS, Fu WM. Prostaglandin E2 stimulates fibronectin expression through EP1 receptor, phospholipase C, protein kinase Calpha, and c-Src pathway in primary cultured rat osteoblasts. J Biol Chem 2005;280:22907-22916.
36. Billot X, Chateauneuf A, Chauret N, Denis D, Greig G, Mathieu MC, Metters KM, Slipetz DM, Young RN. Discovery of a potent and selective agonist of the prostaglandin EP4 receptor. Bioorg Med Chem Lett 2003;13:1129-1132.
37. Jones RL, Giembycz MA, Woodward DF. Prostanoid receptor antagonists: development strategies and therapeutic applications. Br J Pharmacol 2009;158:104-145.
38. Abramovitz M, Adam M, Boie Y, Carri're M, Denis D, Godbout C, Lamontagne S, Rochette C, Sawyer N, Tremblay NM, et al. The utilization of recombinant prostanoid receptors to determine the affinities and selectivities of prostaglandins and related analogs. Biochim Biophys Acta 2000;1483:285-293.
39. Reid G, Wielinga P, Zelcer N, De Haas M, Van Deemter L, Wijnholds J, Balzarini J, Borst P. Characterization of the transport of nucleoside analog drugs by the human multidrug resistance proteins MRP4 and MRP5. Mol Pharmacol 2003;63:1094-1103.
40. Li C, Krishnamurthy PC, Penmatsa H, Marrs KL, Wang XQ, Zaccolo M, Jalink K, Li M, Nelson DJ, Schuetz JD, et al. Spatiotemporal coupling of cAMP transporter to CFTR chloride channel function in the gut epithelia. Cell 2007;131:940-951.
41. Boucher RC. Airway surface dehydration in cystic fibrosis: pathogenesis and therapy. Annu Rev Med 2007;58:157-170.
42. Button B, Picher M, Boucher RC. Differential effects of cyclic and constant stress on ATP release and mucociliary transport by human airway epithelia. J Physiol 2007;580:577-592.
43. Gray T, Coakley R, Hirsh A, Thornton D, Kirkham S, Koo JS, Burch L, Boucher R, Nettesheim P. Regulation of MUC5AC mucin secretion and airway surface liquid metabolism by IL-1beta in human bronchial epithelia. Am J Physiol Lung Cell Mol Physiol 2004;286: L320-L330.
44. Manzanares D, Gonzalez C, Ivonnet P, Chen RS, Valencia-GattasM, Conner GE, Larsson HP, Salathe M. Functional apical large conductance, Ca21-activated, and voltage-dependent K1 channels are required for maintenance of airway surface liquid volume. J BiolChem2011;286:19830-19839.
45. Li C, Naren AP. Analysis of CFTR interactome in the macromolecular complexes. Methods Mol Biol 2011;741:255-270.
46. Li C, Naren AP. CFTR chloride channel in the apical compartments: spatiotemporal coupling to its interacting partners. Integr Biol (Camb) 2010;2:161-177.
47. Ameziane-El-Hassani R, Morand S, Boucher JL, Frapart YM, Apostolou D, Agnandji D, Gnidehou S, Ohayon R, No'l-Hudson MS, Francon J, et al. Dual oxidase-2 has an intrinsic Ca21-dependent H2O2-generating activity. J Biol Chem 2005;280:30046-30054.
48. Okada SF, Zhang L, Kreda SM, Abdullah LH, Davis CW, Pickles RJ, Lazarowski ER, Boucher RC. Coupled nucleotide and mucin hypersecretion from goblet-cell metaplastic human airway epithelium. Am J Respir Cell Mol Biol 2011;45;253-260.
49. Rahman I, Biswas SK, Kode A. Oxidant and antioxidant balance in the airways and airway diseases. Eur J Pharmacol 2006;533:222-239.