Pannexin 1 contributes to ATP release in airway epithelia

American Journal of Respiratory Cell and Molecular Biology

Volumn 41, Issue 5, 2009, Pages 525-534

  Ransford, George A ^a   Fregien, Nevis ^b   Qiu, Feng ^b   Dahl, Gerhard ^b   Conner, Gregory E ^a,b   Salathe, Matthias ^a  

^a UNIVERSITY OF MIAMI   (United States)

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

Author keywords

Airway epithelia; ATP release; Pannexin

Indexed keywords

ADENOSINE TRIPHOSPHATE; CARBENOXOLONE; FLUFENAMIC ACID; MESSENGER RNA; PANNEXIN 1; PROBENECID; PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

AIRWAY; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; LENTIVIRINAE; LUNG ALVEOLUS EPITHELIUM; LUNG ALVEOLUS MACROPHAGE; MUCOCILIARY CLEARANCE; NONHUMAN; PLASMID; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; ANIMALS; CARBENOXOLONE; CELL DEDIFFERENTIATION; CELLS, CULTURED; CONNEXINS; EPITHELIAL CELLS; FLUFENAMIC ACID; GENE EXPRESSION REGULATION; HUMANS; HYPOTONIC SOLUTIONS; MACROPHAGES, ALVEOLAR; MICE; MUCOCILIARY CLEARANCE; NERVE TISSUE PROTEINS; OSMOTIC PRESSURE; PARACRINE COMMUNICATION; PROBENECID; RESPIRATORY MUCOSA; RNA INTERFERENCE; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; TIME FACTORS; TRANSFECTION; XENOPUS;

INVERTEBRATA; LENTIVIRUS;

EID: 70349962258     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2008-0367OC     Document Type: Article

References (60)

1. Morse DM, Smullen JL, Davis CW. Differential effects of UTP, ATP, and adenosine on ciliary activity of human nasal epithelial cells. Am J Physiol 2001;280:C1485-C1497. (Pubitemid 32553204)
2. Lieb T, Wijkstrom Frei C, Frohock JI, Bookman RJ, Salathe M. Prolonged increase in ciliary beat frequency after short-term purinergic stimulation in human airway epithelial cells. J Physiol 2002; 538:633-646. (Pubitemid 35175386)
3. Donaldson SH, Lazarowski ER, Picher M, Knowles MR, Stutts MJ, Boucher RC. Basal nucleotide levels, release, and metabolism in normal and cystic fibrosis airways. Mol Med 2000;6:969-982.
4. 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)
5. Tarran R, Trout L, Donaldson SH, Boucher RC. Soluble mediators, not cilia, determine airway surface liquid volume in normal and cystic fibrosis superficial airway epithelia. J Gen Physiol 2006;127:591-604.
6. Cobb BR, Ruiz F, King CM, Fortenberry J, Greer H, Kovacs T, Sorscher EJ, Clancy JP. A(2) adenosine receptors regulate CFTR through PKA and PLA(2). Am J Physiol Lung Cell Mol Physiol 2002;282:L12-L25.
7. Huang P, Lazarowski ER, Tarran R, Milgram SL, Boucher RC, Stutts MJ. Compartmentalized autocrine signaling to cystic fibrosis transmembrane conductance regulator at the apical membrane of airway epithelial cells. Proc Natl Acad Sci USA 2001;98:14120-14125. (Pubitemid 33116034)
8. 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.
9. Button B, Boucher RC. Role of mechanical stress in regulating airway surface hydration and mucus clearance rates. Respir Physiol Neurobiol 2008;163:189-201.
10. Lazarowski ER, Boucher RC, Harden TK. Constitutive release of ATP and evidence for major contribution of ecto-nucleotide pyrophosphatase and nucleoside diphosphokinase to extracellular nucleotide concentrations. J Biol Chem 2000;275:31061-31068.
11. Zuo P, Picher M, Okada SF, Lazarowski ER, Button B, Boucher RC, Elston TC. Mathematical model of nucleotide regulation on airway epithelia: implications for airway homeostasis. J Biol Chem 2008;283:26805-26819.
12. Lazarowski ER, Shea DA, Boucher RC, Harden TK. Release of cellular UDP-glucose as a potential extracellular signaling molecule. Mol Pharmacol 2003;63:1190-1197.
13. Grygorczyk R, Hanrahan JW. CFTR-independent ATP release from epithelial cells triggered by mechanical stimuli. Am J Physiol 1997; 272:C1058-C1066. (Pubitemid 27146721)
14. Grygorczyk R, Tabcharani JA, Hanrahan JW. CFTR channels expressed in CHO cells do not have detectable ATP conductance. J Membr Biol 1996;151:139-148. (Pubitemid 26194255)
15. Okada SF, O'Neal WK, Huang P, Nicholas RA, Ostrowski LE, Craigen WJ, Lazarowski ER, Boucher RC. Voltage-dependent anion channel-1 (VDAC-1) contributes to ATP release and cell volume regulation in murine cells. J Gen Physiol 2004;124:513-526. (Pubitemid 39506287)
16. Sabirov RZ, Okada Y. Wide nanoscopic pore of maxi-anion channel suits its function as an ATP-conductive pathway. Biophys J 2004;87: 1672-1685. (Pubitemid 39167024)
17. Liu HT, Toychiev AH, Takahashi N, Sabirov RZ, Okada Y. Maxi-anion channel as a candidate pathway for osmosensitive ATP release from mouse astrocytes in primary culture. Cell Res 2008;18:558-565. (Pubitemid 351630947)
18. Evans WH, De Vuyst E, Leybaert L. The gap junction cellular internet: connexin hemichannels enter the signalling limelight. Biochem J 2006; 397:1-14. (Pubitemid 44032830)
19. Stout C, Goodenough DA, Paul DL. Connexins: functions without junctions. Curr Opin Cell Biol 2004;16:507-512.
20. Bao L, Locovei S, Dahl G. Pannexin membrane channels are mechano-sensitive conduits for ATP. FEBS Lett 2004;572:65-68. (Pubitemid 39092514)
21. Locovei S, Wang J, Dahl G. Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett 2006; 580:239-244. (Pubitemid 43005343)
22. Bernacki SH, Nelson AL, Abdullah L, Sheehan JK, Harris A, William Davis C, 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. (Pubitemid 129495647)
23. 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.
24. Fragoso MA, Fernandez V, Forteza R, Randell SH, Salathe M, Conner GE. Transcellular thiocyanate transport by human airway epithelia. J Physiol 2004;561:183-194. (Pubitemid 39549475)
25. Schmid A, Bai G, Schmid N, Zaccolo M, Ostrowski L, Conner G, 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. (Pubitemid 44774024)
26. Mackenzie AB, Chirakkal H, North RA. Kv1.3 potassium channels in human alveolar macrophages. Am J Physiol Lung Cell Mol Physiol 2003;285:L862-L868. (Pubitemid 37158833)
27. Locovei S, Bao L, Dahl G. Pannexin 1 in erythrocytes: function without a gap. Proc Natl Acad Sci USA 2006;103:7655-7659. (Pubitemid 43752836)
28. Zoidl G, Petrasch-Parwez E, Ray A, Meier C, Bunse S, Habbes HW, Dahl G, Dermietzel R. Localization of the pannexin1 protein at postsynaptic sites in the cerebral cortex and hippocampus. Neuroscience 2007;146:9-16. (Pubitemid 46654631)
29. Bruzzone R, Hormuzdi SG, Barbe MT, Herb A, Monyer H. Pannexins, a family of gap junction proteins expressed in brain. Proc Natl Acad Sci USA 2003;100:13644-13649. (Pubitemid 37444793)
30. Penuela S, Bhalla R, Gong XQ, Cowan KN, Celetti SJ, Cowan BJ, Bai D, Shao Q, Laird DW. Pannexin 1 and pannexin 3 are glycoproteins that exhibit many distinct characteristics from the connexin family of gap junction proteins. J Cell Sci 2007;120:3772-3783. (Pubitemid 350187359)
31. Bruzzone R, Barbe MT, Jakob NJ, Monyer H. Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. J Neurochem 2005;92:1033-1043. (Pubitemid 40344294)
32. Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD. The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci USA 2007;104:6436-6441. (Pubitemid 47186112)
33. Tarran R, Button B, Boucher RC. Regulation of normal and cystic fibrosis airway surface liquid volume by phasic shear stress. Annu Rev Physiol 2006;68:543-561.
34. Silverman W, Locovei S, Dahl GP. Probenecid, a gout remedy, inhibits pannexin 1 channels. Am J Physiol Cell Physiol 2008;295:C761-C767.
35. Guyot A, Hanrahan JW. ATP release from human airway epithelial cells studied using a capillary cell culture system. J Physiol 2002;545:199-206. (Pubitemid 35386136)
36. Tarran R, Button B, Picher M, Paradiso AM, Ribeiro CM, Lazarowski ER, Zhang L, Collins PL, Pickles RJ, Fredberg JJ, et al. Normal and cystic fibrosis airway surface liquid homeostasis: the effects of phasic shear stress and viral infections. J Biol Chem 2005;280:35751-35759. (Pubitemid 41532768)
37. Kreda SM, Okada SF, van Heusden CA, O'Neal W, Gabriel S, Abdullah L, Davis CW, Boucher RC, Lazarowski ER. Coordinated release of nucleotides and mucin from human airway epithelial Calu-3 cells. J Physiol 2007;584:245-259. (Pubitemid 47500552)
38. Hansen M, Boitano S, Dirksen ER, Sanderson MJ. Intercellular calcium signaling induced by extracellular adenosine 5′-triphosphate and mechanical stimulation in airway epithelial cells. J Cell Sci 1993;106: 995-1004. (Pubitemid 24018388)
39. Sanderson MJ, Charles AC, Dirksen ER. Mechanical stimulation and intercellular communication increase intracellular calcium in epithelial cells. Cell Regul 1990;1:585-596.
40. Boitano S, Dirksen ER, Sanderson MJ. Intercellular propagation of calcium waves mediated by inositol triphosphate. Science 1992;258:292-295.
41. Boitano S, Dirksen ER, Evans WH. Sequence-specific antibodies to connexins block intercellular calcium signaling through gap junctions. Cell Calcium 1998;23:1-9. (Pubitemid 28159592)
42. Homolya L, Steinberg TH, Boucher RC. Cell to cell communication in response to mechanical stress via bilateral release of ATP and UTP in polarized epithelia. J Cell Biol 2000;150:1349-1360. (Pubitemid 30728907)
43. 2+ signaling in alveolar epithelial cells through gap junctions and by extracellular ATP. Am J Physiol Lung Cell Mol Physiol 2001;280:L221-L228.
44. Cotrina ML, Lin JH, Lopez-Garcia JC, Naus CC, Nedergaard M. ATP-mediated glia signaling. J Neurosci 2000;20:2835-2844.
45. Stout CE, Costantin JL, Naus CC, Charles AC. Intercellular calcium signaling in astrocytes via ATP release through connexin hemi-channels. J Biol Chem 2002;277:10482-10488.
46. Cotrina ML, Lin JH, Alves-Rodrigues A, Liu S, Li J, Azmi-Ghadimi H, Kang J, Naus CC, Nedergaard M. Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci USA 1998; 95:15735-15740. (Pubitemid 29018769)
47. Braet K, Aspeslagh S, Vandamme W, Willecke K, Martin PE, Evans WH, Leybaert L. Pharmacological sensitivity of ATP release triggered by photoliberation of inositol-1,4,5-trisphosphate and zero extracellular calcium in brain endothelial cells. J Cell Physiol 2003;197:205-213.
48. De Vuyst E, Decrock E, Cabooter L, Dubyak GR, Naus CC, Evans WH, Leybaert L. Intracellular calcium changes trigger connexin 32 hemichannel opening. EMBO J 2006;25:34-44. (Pubitemid 43077293)
49. Contreras JE, Saez JC, Bukauskas FF, Bennett MV. Gating and regulation of connexin 43 (Cx43) hemichannels. Proc Natl Acad Sci USA 2003;100:11388-11393.
50. Wang J, Ma M, Locovei S, Keane RW, Dahl G. Modulation of membrane channel currents by gap junction protein mimetic peptides: size matters. Am J Physiol Cell Physiol 2007;293:C1112-C1119. (Pubitemid 47437376)
51. Dahl G. Gap junction-mimetic peptides do work, but in unexpected ways. Cell Commun Adhes 2007;14:259-264. (Pubitemid 351541180)
52. Scemes E, Suadicani SO, Spray DC. Intercellular communication in spinal cord astrocytes: fine tuning between gap junctions and P2 nucleotide receptors in calcium wave propagation. J Neurosci 2000;20: 1435-1445. (Pubitemid 30220423)
53. Wiszniewski L, Sanz J, Scerri I, Gasparotto E, Dudez T, Lacroix JS, Suter S, Gallati S, Chanson M. Functional expression of connexin30 and connexin31 in the polarized human airway epithelium. Differentiation 2007;75:382-392. (Pubitemid 46802160)
54. Bergfeld GR, Forrester T. Release of ATP from human erythrocytes in response to a brief period of hypoxia and hypercapnia. Cardiovasc Res 1992;26:40-47.
55. Sprague RS, Ellsworth ML, Stephenson AH, Kleinhenz ME, Lonigro AJ. Deformation-induced ATP release from red blood cells requires CFTR activity. Am J Physiol 1998;275:H1726-H1732. (Pubitemid 28543706)
56. Dahl G, Locovei S. Pannexin: to gap or not to gap, is that a question? IUBMB Life 2006;58:409-419.
57. Boassa D, Ambrosi C, Qiu F, Dahl G, Gaietta G, Sosinsky G. Pannexin1 channels contain a glycosylation site that targets the hexamer to the plasma membrane. J Biol Chem 2007;282:31733-31743. (Pubitemid 350044851)
58. Boassa D, Qiu F, Dahl G, Sosinsky G. Trafficking dynamics of glycosylated pannexin 1 proteins. Cell Commun Adhes 2008;15:119-132.
59. Loewenstein WR. Junctional intercellular communication: the cell-to-cell membrane channel. Physiol Rev 1981;61:829-913.
60. Mason SJ, Paradiso AM, Boucher RC. Regulation of transepithelial ion transport and intracellular calcium by extracellular ATP in human normal and cystic fibrosis airway epithelium. Br J Pharmacol 1991; 103:1649-1656.