Home LiteratureArticle Details
PMID: 19213873 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Pannexin 1 contributes to ATP release in airway epithelia.

American journal of respiratory cell and molecular biology ·Vol. 41 ·No. 5 ·2009-11-00 ·Pages 525-34

Ransford GA, Fregien N, Qiu F, Dahl G, Conner GE, Salathe M

Abstract

ATP is a paracrine regulator of critical airway epithelial cell functions, but the mechanism of its release is poorly understood. Pannexin (Panx) proteins, related to invertebrate innexins, form channels (called pannexons) that are able to release ATP from several cell types. Thus, ATP release via pannexons was examined in airway epithelial cells. Quantitative RT-PCR showed Panx1 expression in normal human airway epithelial cells during redifferentiation at the air-liquid interface (ALI), at a level comparable to that of alveolar macrophages; Panx3 was not expressed. Immunohistochemistry showed Panx1 expression at the apical pole of airway epithelia. ALI cultures exposed to hypotonic stress released ATP to an estimated maximum of 255 (+/-64) nM within 1 minute after challenge (n = 6 cultures from three different lungs) or to approximately 1.5 (+/-0.4) microM, recalculated to a normal airway surface liquid volume. Using date- and culture-matched cells (each n > or = 16 from 4 different lungs), the pannexon inhibitors carbenoxolone (10 microM) and probenecid (1 mM), but not the connexon inhibitor flufenamic acid (100 microM), inhibited ATP release by approximately 60%. The drugs affected Panx1 currents in Xenopus oocytes expressing exogenous Panx1 correspondingly. In addition, suppression of Panx1 expression using lentivirus-mediated production of shRNA in differentiated airway epithelial cells inhibited ATP release upon hypotonic stress by approximately 60% as well. These data not only show that Panx1 is expressed apically in differentiated airway epithelial cells but also that it contributes to ATP release in these cells.

MeSH Terms
Adenosine Triphosphate/metabolism Animals Carbenoxolone/pharmacology Cell Dedifferentiation Cells, Cultured Connexins/antagonists & inhibitors,genetics,metabolism Epithelial Cells/drug effects,metabolism Flufenamic Acid/pharmacology Gene Expression Regulation Humans Hypotonic Solutions Macrophages, Alveolar/metabolism Mice Mucociliary Clearance Nerve Tissue Proteins/antagonists & inhibitors,genetics,metabolism Osmotic Pressure Paracrine Communication Probenecid/pharmacology RNA Interference RNA, Messenger/metabolism Respiratory Mucosa/drug effects,metabolism Stress, Physiological Time Factors Transfection Xenopus
Chemicals
Connexins Hypotonic Solutions Nerve Tissue Proteins PANX1 protein, human Panx1 protein, mouse RNA, Messenger Flufenamic Acid Adenosine Triphosphate Carbenoxolone Probenecid
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Ransford George A
Division of Pulmonary and Critical Care Medicine (R-47), University of Miami Miller School of Medicine, 1600 NW 10th Ave., RMSB 7058, Miami, FL 33136, USA.
Fregien Nevis
Qiu Feng
Dahl Gerhard
Conner Gregory E
Salathe Matthias
References (60)
60 references, click to expand
  1. Normal and cystic fibrosis airway surface liquid homeostasis. The effects of phasic shear stress and viral infections.
    J Biol Chem. 2005 Oct 21;280(42):35751-9 PMID: 16087672
  2. Intercellular calcium signaling induced by extracellular adenosine 5'-triphosphate and mechanical stimulation in airway epithelial cells.
    J Cell Sci. 1993 Dec;106 ( Pt 4):995-1004 PMID: 8126116
  3. Real-time analysis of cAMP-mediated regulation of ciliary motility in single primary human airway epithelial cells.
    J Cell Sci. 2006 Oct 15;119(Pt 20):4176-86 PMID: 16984973
  4. Transcellular thiocyanate transport by human airway epithelia.
    J Physiol. 2004 Nov 15;561(Pt 1):183-94 PMID: 15345749
  5. Pannexins, a family of gap junction proteins expressed in brain.
    Proc Natl Acad Sci U S A. 2003 Nov 11;100(23):13644-9 PMID: 14597722
  6. Differential effects of UTP, ATP, and adenosine on ciliary activity of human nasal epithelial cells.
    Am J Physiol Cell Physiol. 2001 Jun;280(6):C1485-97 PMID: 11350744
  7. Pannexin1 channels contain a glycosylation site that targets the hexamer to the plasma membrane.
    J Biol Chem. 2007 Oct 26;282(43):31733-43 PMID: 17715132
  8. Gap junction-mimetic peptides do work, but in unexpected ways.
    Cell Commun Adhes. 2007 Nov-Dec;14(6):259-64 PMID: 18392993
  9. Maxi-anion channel as a candidate pathway for osmosensitive ATP release from mouse astrocytes in primary culture.
    Cell Res. 2008 May;18(5):558-65 PMID: 18414449
  10. Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes.
    J Neurochem. 2005 Mar;92(5):1033-43 PMID: 15715654
  11. The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds.
    Proc Natl Acad Sci U S A. 2007 Apr 10;104(15):6436-41 PMID: 17389364
  12. Gating and regulation of connexin 43 (Cx43) hemichannels.
    Proc Natl Acad Sci U S A. 2003 Sep 30;100(20):11388-93 PMID: 13130072
  13. Localization of the pannexin1 protein at postsynaptic sites in the cerebral cortex and hippocampus.
    Neuroscience. 2007 Apr 25;146(1):9-16 PMID: 17379420
  14. ATP-mediated glia signaling.
    J Neurosci. 2000 Apr 15;20(8):2835-44 PMID: 10751435
  15. 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 Nov;197(2):205-13 PMID: 14502560
  16. Connexins: functions without junctions.
    Curr Opin Cell Biol. 2004 Oct;16(5):507-12 PMID: 15363800
  17. ATP release from human airway epithelial cells studied using a capillary cell culture system.
    J Physiol. 2002 Nov 15;545(1):199-206 PMID: 12433960
  18. Pannexin 1 in erythrocytes: function without a gap.
    Proc Natl Acad Sci U S A. 2006 May 16;103(20):7655-9 PMID: 16682648
  19. Compartmentalized autocrine signaling to cystic fibrosis transmembrane conductance regulator at the apical membrane of airway epithelial cells.
    Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):14120-5 PMID: 11707576
  20. Mathematical model of nucleotide regulation on airway epithelia. Implications for airway homeostasis.
    J Biol Chem. 2008 Sep 26;283(39):26805-19 PMID: 18662982
  21. Physiological regulation of ATP release at the apical surface of human airway epithelia.
    J Biol Chem. 2006 Aug 11;281(32):22992-3002 PMID: 16754672
  22. Intercellular communication in spinal cord astrocytes: fine tuning between gap junctions and P2 nucleotide receptors in calcium wave propagation.
    J Neurosci. 2000 Feb 15;20(4):1435-45 PMID: 10662834
  23. Deformation-induced ATP release from red blood cells requires CFTR activity.
    Am J Physiol. 1998 Nov;275(5):H1726-32 PMID: 9815080
  24. Coordinated release of nucleotides and mucin from human airway epithelial Calu-3 cells.
    J Physiol. 2007 Oct 1;584(Pt 1):245-59 PMID: 17656429
  25. Soluble mediators, not cilia, determine airway surface liquid volume in normal and cystic fibrosis superficial airway epithelia.
    J Gen Physiol. 2006 May;127(5):591-604 PMID: 16636206
  26. Cell to cell communication in response to mechanical stress via bilateral release of ATP and UTP in polarized epithelia.
    J Cell Biol. 2000 Sep 18;150(6):1349-60 PMID: 10995440
  27. Prolonged increase in ciliary beat frequency after short-term purinergic stimulation in human airway epithelial cells.
    J Physiol. 2002 Jan 15;538(Pt 2):633-46 PMID: 11790825
  28. Release of cellular UDP-glucose as a potential extracellular signaling molecule.
    Mol Pharmacol. 2003 May;63(5):1190-7 PMID: 12695547
  29. Pannexin membrane channels are mechanosensitive conduits for ATP.
    FEBS Lett. 2004 Aug 13;572(1-3):65-8 PMID: 15304325
  30. Mechanical stimulation and intercellular communication increases intracellular Ca2+ in epithelial cells.
    Cell Regul. 1990 Jul;1(8):585-96 PMID: 2078569
  31. Probenecid, a gout remedy, inhibits pannexin 1 channels.
    Am J Physiol Cell Physiol. 2008 Sep;295(3):C761-7 PMID: 18596212
  32. Intercellular propagation of calcium waves mediated by inositol trisphosphate.
    Science. 1992 Oct 9;258(5080):292-5 PMID: 1411526
  33. Intracellular calcium changes trigger connexin 32 hemichannel opening.
    EMBO J. 2006 Jan 11;25(1):34-44 PMID: 16341088
  34. Connexins regulate calcium signaling by controlling ATP release.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15735-40 PMID: 9861039
  35. Intercellular Ca2+ signaling in alveolar epithelial cells through gap junctions and by extracellular ATP.
    Am J Physiol Lung Cell Mol Physiol. 2001 Feb;280(2):L221-8 PMID: 11159000
  36. Role of mechanical stress in regulating airway surface hydration and mucus clearance rates.
    Respir Physiol Neurobiol. 2008 Nov 30;163(1-3):189-201 PMID: 18585484
  37. Regulation of transepithelial ion transport and intracellular calcium by extracellular ATP in human normal and cystic fibrosis airway epithelium.
    Br J Pharmacol. 1991 Jul;103(3):1649-56 PMID: 1718521
  38. Mucin gene expression during differentiation of human airway epithelia in vitro. Muc4 and muc5b are strongly induced.
    Am J Respir Cell Mol Biol. 1999 Apr;20(4):595-604 PMID: 10100990
  39. CFTR-independent ATP release from epithelial cells triggered by mechanical stimuli.
    Am J Physiol. 1997 Mar;272(3 Pt 1):C1058-66 PMID: 9124508
  40. Regulation of normal and cystic fibrosis airway surface liquid volume by phasic shear stress.
    Annu Rev Physiol. 2006;68:543-61 PMID: 16460283
  41. Modulation of membrane channel currents by gap junction protein mimetic peptides: size matters.
    Am J Physiol Cell Physiol. 2007 Sep;293(3):C1112-9 PMID: 17652431
  42. Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels.
    J Biol Chem. 2002 Mar 22;277(12):10482-8 PMID: 11790776
  43. Nucleotide release provides a mechanism for airway surface liquid homeostasis.
    J Biol Chem. 2004 Aug 27;279(35):36855-64 PMID: 15210701
  44. Junctional intercellular communication: the cell-to-cell membrane channel.
    Physiol Rev. 1981 Oct;61(4):829-913 PMID: 6270711
  45. The gap junction cellular internet: connexin hemichannels enter the signalling limelight.
    Biochem J. 2006 Jul 1;397(1):1-14 PMID: 16761954
  46. 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 Oct;27(4):436-45 PMID: 12356577
  47. CFTR channels expressed in CHO cells do not have detectable ATP conductance.
    J Membr Biol. 1996 May;151(2):139-48 PMID: 8661502
  48. Voltage-dependent anion channel-1 (VDAC-1) contributes to ATP release and cell volume regulation in murine cells.
    J Gen Physiol. 2004 Nov;124(5):513-26 PMID: 15477379
  49. Basal nucleotide levels, release, and metabolism in normal and cystic fibrosis airways.
    Mol Med. 2000 Nov;6(11):969-82 PMID: 11147574
  50. Sequence-specific antibodies to connexins block intercellular calcium signaling through gap junctions.
    Cell Calcium. 1998 Jan;23(1):1-9 PMID: 9570005
  51. Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium.
    FEBS Lett. 2006 Jan 9;580(1):239-44 PMID: 16364313
  52. Release of ATP from human erythrocytes in response to a brief period of hypoxia and hypercapnia.
    Cardiovasc Res. 1992 Jan;26(1):40-7 PMID: 1325292
  53. Pannexin 1 and pannexin 3 are glycoproteins that exhibit many distinct characteristics from the connexin family of gap junction proteins.
    J Cell Sci. 2007 Nov 1;120(Pt 21):3772-83 PMID: 17925379
  54. Kv1.3 potassium channels in human alveolar macrophages.
    Am J Physiol Lung Cell Mol Physiol. 2003 Oct;285(4):L862-8 PMID: 12909584
  55. Pannexin: to gap or not to gap, is that a question?
    IUBMB Life. 2006 Jul;58(7):409-19 PMID: 16801216
  56. Constitutive release of ATP and evidence for major contribution of ecto-nucleotide pyrophosphatase and nucleoside diphosphokinase to extracellular nucleotide concentrations.
    J Biol Chem. 2000 Oct 6;275(40):31061-8 PMID: 10913128
  57. Wide nanoscopic pore of maxi-anion channel suits its function as an ATP-conductive pathway.
    Biophys J. 2004 Sep;87(3):1672-85 PMID: 15345546
  58. Functional expression of connexin30 and connexin31 in the polarized human airway epithelium.
    Differentiation. 2007 Jun;75(5):382-92 PMID: 17428265
  59. Trafficking dynamics of glycosylated pannexin 1 proteins.
    Cell Commun Adhes. 2008 May;15(1):119-32 PMID: 18649184
  60. A(2) adenosine receptors regulate CFTR through PKA and PLA(2).
    Am J Physiol Lung Cell Mol Physiol. 2002 Jan;282(1):L12-25 PMID: 11741811
Article Info
Journal
American journal of respiratory cell and molecular biology
Abbr.
Am J Respir Cell Mol Biol
ISSN
1535-4989
Published
2009-11-00
Epub
2009-00-12
Pages
525-34
Language
English
Region
United States
NLM ID
8917225
PMCID
PMC2778159
Subset
IM
Grants
NHLBI NIH HHS · HL-66125 · United States
NHLBI NIH HHS · R01 HL089399-02 · United States
NHLBI NIH HHS · R01 HL089399 · United States
NHLBI NIH HHS · HL-89399 · United States
NIGMS NIH HHS · GM-48610 · United States
NHLBI NIH HHS · R01 HL060644-10 · United States
NHLBI NIH HHS · HL-60644 · United States
NIGMS NIH HHS · R01 GM048610 · United States
NHLBI NIH HHS · R01 HL060644 · United States
NIGMS NIH HHS · R01 GM048610-15 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]