A P2X Ion Channel-triggered NF-{kappa}B Pathway Enhances TNF-{alpha}-induced IL-8 Expression in Airway Epithelial Cells.

Theatre, Emilie; Bours, Vincent; Oury, Cécile

doi:10.1165/rcmb.2008-0452OC

Article (Scientific journals)

A P2X Ion Channel-triggered NF-{kappa}B Pathway Enhances TNF-{alpha}-induced IL-8 Expression in Airway Epithelial Cells.

Theatre, Emilie; Bours, Vincent; Oury, Cécile

2009 • In American Journal of Respiratory Cell and Molecular Biology

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/20341

DOI
10.1165/rcmb.2008-0452OC

PubMed
19265173

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Theatre et al in press.pdf

Author preprint (655.13 kB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

airway inflammation; purinergic receptors; NF-kappaB

Abstract :

[en] Extracellular ATP, acting at P2Y and P2X receptors, has recently been shown to contribute to airway inflammation. Using different epithelial cell models, this study shows that ATP promotes TNF-alpha-elicited IL-8 expression through P2X ion channel-triggered Ca(2+) entry, leading to CaMK-dependent IKK activation and binding of active p65 to IL-8 gene promoter.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Theatre, Emilie ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > GIGA-R : Génétique générale et humaine

Bours, Vincent ; Université de Liège - ULiège > Génétique

Oury, Cécile ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > GIGA-R : Génétique générale et humaine

Language :

English

Title :

A P2X Ion Channel-triggered NF-{kappa}B Pathway Enhances TNF-{alpha}-induced IL-8 Expression in Airway Epithelial Cells.

Publication date :

2009

Journal title :

American Journal of Respiratory Cell and Molecular Biology

ISSN :

1044-1549

eISSN :

1535-4989

Publisher :

American Thoracic Society, New York, United States - New York

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 28 August 2009

Statistics

Number of views

139 (33 by ULiège)

Number of downloads

0 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Lazarowski ER, Boucher RC, Harden TK. Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol Pharmacol 2003;64:785-795.
Burnstock G. Purine and pyrimidine receptors. Cell Mol Life Sci 2007; 64:1471-1483.
Khakh BS, North RA. P2X receptors as cell-surface ATP sensors in health and disease. Nature 2006;442:527-532.
North RA. Molecular physiology of P2X receptors. Physiol Rev 2002;82: 1013-1067.
Torres GE, Egan TM, Voigt MM. Hetero-oligomeric assembly of P2X receptor subunits: specificities exist with regard to possible partners. J Biol Chem 1999;274:6653-6659.
Lazarowski ER, Tarran R, Grubb BR, van Heusden CA, Okada S, Boucher RC. Nucleotide release provides a mechanism for airway surface liquid homeostasis. J Biol Chem 2004;279:36855-36864. (Pubitemid 39129034)
Schwiebert EM, Zsembery A. Extracellular ATP as a signaling molecule for epithelial cells. Biochim Biophys Acta 2003;1615:7-32. (Pubitemid 37013465)
Stutts MJ, Chinet TC, Mason SJ, Fullton JM, Clarke LL, Boucher RC. Regulation of Cl- channels in normal and cystic fibrosis airway epithelial cells by extracellular ATP. Proc Natl Acad Sci USA 1992; 89:1621-1625.
Taylor AL, Schwiebert LM, Smith JJ, King C, Jones JR, Sorscher EJ, Schwiebert EM. Epithelial P2X purinergic receptor channel expression and function. J Clin Invest 1999;104:875-884. (Pubitemid 29536337)
Clarke LL, Chinet T, Boucher RC. Extracellular ATP stimulates K + secretion across cultured human airway epithelium. Am J Physiol 1997;272:L1084-L1091.
Jiang C, Finkbeiner WE, Widdicombe JH, McCray PB Jr, Miller SS. Altered fluid transport across airway epithelium in cystic fibrosis. Science 1993;262:424-427. (Pubitemid 23353385)
Mall M, Wissner A, Gonska T, Calenborn D, Kuehr J, Brandis M, Kunzelmann K. Inhibition of amiloride-sensitive epithelial Na(+) absorption by extracellular nucleotides in human normal and cystic fibrosis airways. Am J Respir Cell Mol Biol 2000;23:755-761. (Pubitemid 32013267)
Hayashi T, Kawakami M, Sasaki S, Katsumata T, Mori H, Yoshida H, Nakahari T. ATP regulation of ciliary beat frequency in rat tracheal and distal airway epithelium. Exp Physiol 2005;90:535-544. (Pubitemid 40980154)
Okada SF, Nicholas RA, Kreda SM, Lazarowski ER, Boucher RC. Physiological regulation of ATP release at the apical surface of human airway epithelia. J Biol Chem 2006;281:22992-23002.
Davis CW, Dowell ML, Lethem M, Van Scott M. Goblet cell degranulation in isolated canine tracheal epithelium: response to exogenous ATP, ADP, and adenosine. Am J Physiol 1992;262: C1313-C1323.
Kunzelmann K, Mall M. Pharmacotherapy of the ion transport defect in cystic fibrosis: role of purinergic receptor agonists and other potential therapeutics. Am J Respir Med 2003;2:299-309. (Pubitemid 37045675)
Ma W, Korngreen A, Weil S, Cohen EB, Priel A, Kuzin L, Silberberg SD. Pore properties and pharmacological features of the P2X receptor channel in airway ciliated cells. J Physiol 2006;571:503-517. (Pubitemid 43329544)
Kellerman D, Evans R, Mathews D, Shaffer C. Inhaled P2Y2 receptor agonists as a treatment for patients with cystic fibrosis lung disease. Adv Drug Deliv Rev 2002;54:1463-1474. (Pubitemid 35375770)
Burnstock G. Pathophysiology and therapeutic potential of purinergic signaling. Pharmacol Rev 2006;58:58-86. (Pubitemid 43313697)
Zsembery A, Fortenberry JA, Liang L, Bebok Z, Tucker TA, Boyce AT, Braunstein GM, Welty E, Bell PD, Sorscher EJ, et al. Extracellular zinc and ATP restore chloride secretion across cystic fibrosis airway epithelia by triggering calcium entry. J Biol Chem 2004;279:10720-10729.
Bours MJ, Swennen EL, Di Virgilio F, Cronstein BN, Dagnelie PC. Adenosine 5′-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol Ther 2006;112: 358-404. (Pubitemid 44486409)
Idzko M, Panther E, Bremer HC, Sorichter S, Luttmann W, Virchow CJ Jr, Di Virgilio F, Herouy Y, Norgauer J, Ferrari D. Stimulation of P2 purinergic receptors induces the release of eosinophil cationic protein and interleukin-8 from human eosinophils. Br J Pharmacol 2003;138: 1244-1250. (Pubitemid 36543121)
Khine AA, Del Sorbo L, Vaschetto R, Voglis S, Tullis E, Slutsky AS, Downey GP, Zhang H. Human neutrophil peptides induce interleukin-8 production through the P2Y6 signaling pathway. Blood 2006; 107:2936-2942.
Fu Z, Bettega K, Carroll S, Buchholz KR, Machen TE. Role of Ca 2+ in responses of airway epithelia to Pseudomonas aeruginosa, flagellin, ATP, and thapsigargin. Am J Physiol Lung Cell Mol Physiol 2007; 292:L353-L364.
Baggiolini M, Clark-Lewis I. Interleukin-8, a chemotactic and inflammatory cytokine. FEBS Lett 1992;307:97-101.
Bonfield TL, Konstan MW, Berger M. Altered respiratory epithelial cell cytokine production in cystic fibrosis. J Allergy Clin Immunol 1999; 104:72-78. (Pubitemid 29364482)
Sun Y, Wu F, Sun F, Huang P. Adenosine promotes IL-6 release in airway epithelia. J Immunol 2008;180:4173-4181.
Douillet CD, Robinson WP III, Milano PM, Boucher RC, Rich PB. Nucleotides induce IL-6 release from human airway epithelia via P2Y2 and p38 MAPK-dependent pathways. Am J Physiol Lung Cell Mol Physiol 2006;291:L734-L746.
Idzko M, Hammad H, van Nimwegen M, Kool M, Willart MA, Muskens F, Hoogsteden HC, Luttmann W, Ferrari D, Di Virgilio F, et al. Extracellular ATP triggers and maintains asthmatic airway inflammation by activating dendritic cells. Nat Med 2007;13:913-919. (Pubitemid 47222044)
Gever JR, Cockayne DA, Dillon MP, Burnstock G, Ford AP. Pharmacology of P2X channels. Pflugers Arch 2006;452:513-537.
Stein B, Baldwin AS Jr. Distinct mechanisms for regulation of the interleukin-8 gene involve synergism and cooperativity between C/EBP and NF-kappa B. Mol Cell Biol 1993;13:7191-7198. (Pubitemid 23321171)
Hoffmann E, Dittrich-Breiholz O, Holtmann H, Kracht M. Multiple control of interleukin-8 gene expression. J Leukoc Biol 2002;72:847-855. (Pubitemid 35365158)
Ratner AJ, Bryan R, Weber A, Nguyen S, Barnes D, Pitt A, Gelber S, Cheung A, Prince A. Cystic fibrosis pathogens activate Ca2+-dependent mitogen-activated protein kinase signaling pathways in airway epithelial cells. J Biol Chem 2001;276:19267-19275.
Hayden MS, Ghosh S. Signaling to NF-kappaB. Genes Dev 2004;18: 2195-2224.
McNamara N, Gallup M, Sucher A, Maltseva I, McKemy D, Basbaum C. AsialoGM1 and TLR5 cooperate in flagellin-induced nucleotide signaling to activate Erk1/2. Am J Respir Cell Mol Biol 2006;34:653-660. (Pubitemid 43825328)
Liang L, Zsembery A, Schwiebert EM. RNA interference targeted to multiple P2X receptor subtypes attenuates zinc-induced calcium entry. Am J Physiol Cell Physiol 2005;289:C388-C396.
Lambrecht G. Agonists and antagonists acting at P2X receptors: selectivity profiles and functional implications. Naunyn Schmiedebergs Arch Pharmacol 2000;362:340-350.
Lilienbaum A, Israel A. From calcium to NF-kappa B signaling pathways in neurons. Mol Cell Biol 2003;23:2680-2698. (Pubitemid 36403070)
Viatour P, Merville MP, Bours V, Chariot A. Phosphorylation of NFkappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem Sci 2005;30:43-52. (Pubitemid 40093740)
Le KT, Babinski K, Seguela P. Central P2X4 and P2X6 channel subunits coassemble into a novel heteromeric ATP receptor. J Neurosci 1998; 18:7152-7159. (Pubitemid 28425802)
Guo C, Masin M, Qureshi OS, Murrell-Lagnado RD. Evidence for functional P2X4/P2X7 heteromeric receptors. Mol Pharmacol 2007; 72:1447-1456.
Aga M, Watters JJ, Pfeiffer ZA, Wiepz GJ, Sommer JA, Bertics PJ. Evidence for nucleotide receptor modulation of cross talk between MAP kinase and NF-kappa B signaling pathways in murine RAW 264.7 macrophages. Am J Physiol Cell Physiol 2004;286:C923-C930.
Budagian V, Bulanova E, Brovko L, Orinska Z, Fayad R, Paus R, Bulfone-Paus S. Signaling through P2X7 receptor in human T cells involves p56lck, MAP kinases, and transcription factors AP-1 and NF-kappa B. J Biol Chem 2003;278:1549-1560.
Ferrari D, Wesselborg S, Bauer MK, Schulze-Osthoff K. Extracellular ATP activates transcription factor NF-kappaB through the P2Z purinoreceptor by selectively targeting NF-kappaB p65. J Cell Biol 1997;139:1635-1643. (Pubitemid 28079229)
Korcok J, Raimundo LN, Ke HZ, Sims SM, Dixon SJ. Extracellular nucleotides act through P2X7 receptors to activate NF-kappaB in osteoclasts. J Bone Miner Res 2004;19:642-651. (Pubitemid 41071225)
Kim YM, Reed W, Wu W, Bromberg PA, Graves LM, Samet JM. Zn 2+-induced IL-8 expression involves AP-1, JNK, and ERK activities in human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2006;290:L1028-L1035.
Kim YM, Cao D, Reed W, Wu W, Jaspers I, Tal T, Bromberg PA, Samet JM. Zn2+-induced NF-kappaB-dependent transcriptional activity involves site-specific p65/RelA phosphorylation. Cell Signal 2007;19: 538-546. (Pubitemid 46107805)
Jang MK, Goo YH, Sohn YC, Kim YS, Lee SK, Kang H, Cheong J, Lee JW. Ca2+/calmodulin-dependent protein kinase IV stimulates nuclear factor-kappa B transactivation via phosphorylation of the p65 subunit. J Biol Chem 2001;276:20005-20010.
Hughes K, Edin S, Antonsson A, Grundstrom T. Calmodulin-dependent kinase II mediates T cell receptor/CD3- and phorbol ester-induced activation of IkappaB kinase. J Biol Chem 2001;276:36008-36013.
Ishiguro K, Green T, Rapley J, Wachtel H, Giallourakis C, Landry A, Cao Z, Lu N, Takafumi A, Goto H, et al. Ca2+/calmodulin-dependent protein kinase II is a modulator of CARMA1-mediated NF-kappaB activation. Mol Cell Biol 2006;26:5497-5508.
Wegener E, Krappmann D. CARD-Bcl10-Malt1 signalosomes: missing link to NF-kappaB. Sci STKE 2007;384:pe21.
Schafer R, Sedehizade F, Welte T, Reiser G. ATP- and UTP-activated P2Y receptors differently regulate proliferation of human lung epithelial tumor cells. Am J Physiol Lung Cell Mol Physiol 2003; 285:L376-L385. (Pubitemid 36909454)
Newton R, Holden NS, Catley MC, Oyelusi W, Leigh R, Proud D, Barnes PJ. Repression of inflammatory gene expression in human pulmonary epithelial cells by small-molecule IkappaB kinase inhibitors. J Pharmacol Exp Ther 2007;321:734-742. (Pubitemid 46624511)
Berry M, Brightling C, Pavord I, Wardlaw A. TNF-alpha in asthma. Curr Opin Pharmacol 2007;7:279-282.
Lykouras D, Sampsonas F, Kaparianos A, Karkoulias K, Spiropoulos K. Role and pharmacogenomics of TNF-alpha in asthma. Mini Rev Med Chem 2008;8:934-942.