Nitric oxide inhibits highly selective sodium channels and the Na +/K+-ATPase in H441 cells

American Journal of Respiratory Cell and Molecular Biology

Volumn 44, Issue 1, 2010, Pages 53-65

  Althaus, Mike ^a   Pichl, Alexandra ^a   Clauss, Wolfgang G ^a   Seeger, Werner ^a   Fronius, Martin ^a   Morty, Rory E ^a  

^a JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

Author keywords

Alveolar epithelium; Na+ K + ATPase; NaC; Nitric oxide; Sodium transport

Indexed keywords

1 [N (3 AMINOPROPYL) N (N PROPYL)AMINO]DIAZEN 1 IUM 1,2 DIOLATE; 1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 8 BROMO CYCLIC GMP; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AMILORIDE; BIOTIN; DIETHYLAMMONIUM 1 (N,N DIETHYLAMINO)DIAZEN 1 IUM 1,2 DIOLATE; GUANYLATE CYCLASE; GUANYLATE CYCLASE INHIBITOR; HEMOGLOBIN; MERCURY; METHYLENE BLUE; N ETHYLMALEIMIDE; NITRIC OXIDE; NITRIC OXIDE DONOR; SODIUM CHANNEL; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN; CELL STRAIN H441; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN TISSUE; ION TRANSPORT; MONOLAYER CULTURE; PROTEIN EXPRESSION; SODIUM ABSORPTION; WESTERN BLOTTING; XENOPUS;

AMILORIDE; ANIMALS; BIOTINYLATION; BLOTTING, WESTERN; BRONCHIOLES; CELL LINE; CYCLIC GMP; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; EPITHELIAL CELLS; EPITHELIAL SODIUM CHANNEL; GUANYLATE CYCLASE; HEMOGLOBINS; HUMANS; HYDRAZINES; MEMBRANE POTENTIALS; NITRIC OXIDE; NITRIC OXIDE DONORS; PATCH-CLAMP TECHNIQUES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SODIUM; SODIUM CHANNEL BLOCKERS; SODIUM-POTASSIUM-EXCHANGING ATPASE; SULFHYDRYL COMPOUNDS; XENOPUS;

EID: 78650638452     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/2009-0335OC     Document Type: Article

References (67)

1. Furchgott RF, Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 1980;288:373-376.
2. Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987;327:524-526. (Pubitemid 17085822)
3. Shaul PW. Regulation of endothelial nitric oxide synthase: location, location, location. Annu Rev Physiol 2002;64:749-774.
4. Giaid A, Saleh D. Reduced expression of endothelial nitric oxide synthase in the lungs of patients with pulmonary hypertension. N Engl J Med 1995;333:214-221.
5. Xue C, Botkin SJ, Johns RA. Localization of endothelial NOS at the basal microtubule membrane in ciliated epithelium of rat lung. J Histochem Cytochem 1996;44:463-471.
6. Kelley TJ, Drumm ML. Inducible nitric oxide synthase expression is reduced in cystic fibrosis murine and human airway epithelial cells. J Clin Invest 1998;102:1200-1207.
7. Haddad IY, Pataki G, Hu P, Galliani C, Beckman JS, Matalon S. Quantitation of nitrotyrosine levels in lung sections of patients and animals with acute lung injury. J Clin Invest 1994;94:2407-2413.
8. Kobayashi A, Hashimoto S, Kooguchi K, Kitamura Y, Onodera H, Urata Y, Ashihara T. Expression of inducible nitric oxide synthase and inflammatory cytokines in alveolar macrophages of ARDS following sepsis. Chest 1998;113:1632-1639.
9. Sittipunt C, Steinberg KP, Ruzinski JT, Myles C, Zhu S, Goodman RB, Hudson LD, Matalon S, Martin TR. Nitric oxide and nitrotyrosine in the lungs of patients with acute respiratory distress syndrome. Am J Respir Crit Care Med 2001;163:503-510.
10. Elphick HE, Demoncheaux EA, Ritson S, Higenbottam TW, Everard ML. Exhaled nitric oxide is reduced in infants with cystic fibrosis. Thorax 2001;56:151-152.
11. Massaro AF, Mehta S, Lilly CM, Kobzik L, Reilly JJ, Drazen JM. Elevated nitric oxide concentrations in isolated lower airway gas of asthmatic subjects. Am J Respir Crit Care Med 1996;153:1510-1514.
12. Morty RE, Eickelberg O, Seeger W. Alveolar fluid clearance in acute lung injury: what have we learned from animal models and clinical studies? Intensive Care Med 2007;33:1229-1240.
13. Kaestle SM, Reich CA, Yin N, Habazettl H, Weimann J, Kuebler WM. Nitric oxide-dependent inhibition of alveolar fluid clearance in hydrostatic lung edema. Am J Physiol Lung Cell Mol Physiol 2007; 293:L859-L869.
14. Nielsen VG, Baird MS, Chen L, Matalon S. DETANONOate, a nitric oxide donor, decreases amiloride-sensitive alveolar fluid clearance in rabbits. Am J Respir Crit Care Med 2000;161:1154-1160.
15. Matthay MA, Folkesson HG, Clerici C. Lung epithelial fluid transport and the resolution of pulmonary edema. Physiol Rev 2002;82: 569-600.
16. Guo Y, DuVall MD, Crow JP, Matalon S. Nitric oxide inhibits Na+ absorption across cultured alveolar type II monolayers. Am J Physiol 1998;274:L369-L377.
17. Jain L, Chen XJ, Brown LA, Eaton DC. Nitric oxide inhibits lung sodium transport through a cGMP-mediated inhibition of epithelial cation channels. Am J Physiol 1998;274:L475-L484.
18. Helms MN, Yu L, Malik B, Kleinhenz DJ, Hart CM, Eaton DC. Role of SGK1 in nitric oxide inhibition of ENaC in Na+-transporting epithelia. Am J Physiol Cell Physiol 2005;289:C717-C726.
19. Matalon S, Lazrak A, Jain L, Eaton DC. Invited review: biophysical properties of sodium channels in lung alveolar epithelial cells. J Appl Physiol 2002;93:1852-1859.
20. Helms MN, Jain L, Self JL, Eaton DC. Redox regulation of epithelial sodium channels (ENaC) examined in alveolar type 1 and 2 cells patch clamped in lung slice tissue. J Biol Chem 2008;283:22875-22883.
21. Matalon S, Hardiman KM, Jain L, Eaton DC, Kotlikoff M, Eu JP, Sun J, Meissner G, Stamler JS. Regulation of ion channel structure and function by reactive oxygen-nitrogen species. Am J Physiol Lung Cell Mol Physiol 2003;285:L1184-L1189.
22. Brown SG, Gallacher M, Olver RE, Wilson SM. The regulation of selective and nonselective Na+ conductances in H441 human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2008;294:L942-L954.
23. Ji HL, Su XF, Kedar S, Li J, Barbry P, Smith PR, Matalon S, Benos DJ. Delta-subunit confers novel biophysical features to alpha beta gamma-human epithelial sodium channel (ENaC) via a physical interaction. J Biol Chem 2006;281:8233-8241.
24. Ramminger SJ, Richard K, Inglis SK, Land SC, Olver RE, Wilson SM. A regulated apical Na(+) conductance in dexamethasone-treated H441 airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2004;287: L411-L419.
25. Woollhead AM, Baines DL. Forskolin-induced cell shrinkage and apical translocation of functional enhanced green fluorescent protein-human alphaENaC in H441 lung epithelial cell monolayers. J Biol Chem 2006;281:5158-5168.
26. Woollhead AM, Scott JW, Hardie DG, Baines DL. Phenformin and 5-aminoimidazole-4-carboxamide-1-beta-D-ribofuranoside (AICAR) activation of AMP-activated protein kinase inhibits transepithelial Na+ transport across H441 lung cells. J Physiol 2005;566:781-792.
27. Althaus M, Fronius M, Buchackert Y, Vadasz I, Clauss WG, Seeger W, Motterlini R, Morty RE. Carbon monoxide rapidly impairs alv eolarfluid clearance by inhibiting epithelial sodium channels. Am J Respir Cell Mol Biol 2009;41:639-650.
28. Fronius M, Bogdan R, Althaus M, Morty RE, Clauss WG. Epithelial Na(+) channels derived from human lung are activated by shear force. Respir Physiol Neurobiol 2010;170:113-119.
29. Althaus M, Bogdan R, Clauss WG, Fronius M. Mechano-sensitivity of epithelial sodium channels (ENaCs): laminar shear stress increase esion channel open probability. FASEB J 2007;10:2389-2399.
30. Jaffrey SR, Snyder SH. The biotin switch method for the detection of S-nitrosylated proteins. Sci STKE 2001;2001:p11.
31. Chen L, Song W, Davis IC, Shrestha K, Schwiebert E, Sullender WM, Matalon S. Inhibition of Na+ transport in lung epithelial cells by respiratory syncytial virus infection. Am J Respir Cell Mol Biol 2009; 40:588-600.
32. Kulaksiz H, Schmid A, Honscheid M, Ramaswamy A, Cetin Y. Clara cell impact in air-side activation of CFTR in small pulmonary airways. Proc Natl Acad Sci USA 2002;99:6796-6801.
33. Lazrak A, Matalon S. cAMP-induced changes of apical membrane potentials of confluent H441 monolayers. Am J Physiol Lung Cell Mol Physiol 2003;285:L443-L450.
34. Wilson SM, Brown SG, McTavish N, McNeill RP, Husband EM, Inglis SK, Olver RE, Clunes MT. Expression of intermediate-conductance, Ca2+-activated K+ channel (KCNN4) in H441 human distal airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2006; 291:L957-L965.
35. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 1996;271:C1424-C1437.
36. Furchgott RF, Vanhoutte PM. Endothelium-derived relaxing and contracting factors. FASEB J 1989;3:2007-2018.
37. Albert AP, Woollhead AM, Mace OJ, Baines DL. AICAR decreases the activity of two distinct amiloride-sensitive Na+-permeable channels in H441 human lung epithelial cell monolayers. Am J Physiol Lung Cell Mol Physiol 2008;295:L837-L848.
38. Chraibi A, Horisberger JD. Dual effect of temperature on the human epithelial Na+ channel. Pflugers Arch 2003;447:316-320.
39. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 2001;3:193-197.
40. Sato T, Kamata Y, Irifune M, Nishikawa T. Inhibition of purified (Na+,K+)-ATPase activity from porcine cerebral cortex by NO generating drugs. Brain Res 1995;704:117-120.
41. Saville B. A scheme for the colorimetric determination of microgram amounts of thiols. Analyst (Lond) 1958;83:670-672.
42. Maejima Y, Adachi S, Morikawa K, Ito H, Isobe M. Nitric oxide inhibits myocardial apoptosis by preventing caspase-3 activity via S-nitrosylation. J Mol Cell Cardiol 2005;38:163-174.
43. Simon DI, Mullins ME, Jia L, Gaston B, Singel DJ, Stamler JS. Polynitrosylated proteins: characterization, bioactivity, and functional consequences. Proc Natl Acad Sci USA 1996;93:4736-4741.
44. Stamler JS, Lamas S, Fang FC. Nitrosylation: the prototypic redox-based signaling mechanism. Cell 2001;106:675-683.
45. Barrett DM, Black SM, Todor H, Schmidt-Ullrich RK, Dawson KS, Mikkelsen RB. Inhibition of protein-tyrosine phosphatases by mild oxidative stresses is dependent on S-nitrosylation. J Biol Chem 2005; 280:14453-14461.
46. Duszyk M, Radomski MW. The role of nitric oxide in the regulation of ion channels in airway epithelium: implications for diseases of the lung. Free Radic Res 2000;33:449-459.
47. Song W, Matalon S. Modulation of alveolar fluid clearance by reactive oxygen-nitrogen intermediates. Am J Physiol Lung Cell Mol Physiol 2007;293:L855-L858.
48. Chen L, Bosworth CA, Pico T, Collawn JF, Varga K, Gao Z, Clancy JP, Fortenberry JA, Lancaster JRJ, Matalon S. DETANO and nitrated lipids increase chloride secretion across lung airway cells. Am J Respir Cell Mol Biol 2008;39:150-162.
49. Kamosinska B, Radomski MW, Duszyk M, Radomski A, Man SF. Nitric oxide activates chloride currents in human lung epithelial cells. Am J Physiol 1997;272:L1098-L1104.
50. Lazrak A, Samanta A, Matalon S. Biophysical properties and molecular characterization of amiloride-sensitive sodium channels in A549 cells. Am J Physiol Lung Cell Mol Physiol 2000;278:L848-L857.
51. Hu P, Ischiropoulos H, Beckman JS, Matalon S. Peroxynitrite inhibition of oxygen consumption and sodium transport in alveolar type II cells. Am J Physiol 1994;266:L628-L634.
52. Pittet JF, Lu LN, Morris DG, Modelska K, Welch WJ, Carey HV, Roux J, Matthay MA. Reactive nitrogen species inhibit alveolar epithelial fluid transport after hemorrhagic shock in rats. J Immunol 2001;166: 6301-6310.
53. DuVall MD, Zhu S, Fuller CM, Matalon S. Peroxynitrite inhibits amiloride-sensitive Na+ currents in Xenopus oocytes expressing alpha beta gamma-rENaC. Am J Physiol 1998;274:C1417-C1423.
54. Nie HG, Chen L, Han DY, Li J, Song WF, Wei SP, Fang XH, Gu X, Matalon S, Ji HL. Regulation of epithelial sodium channels by cGMP/ PKGII. J Physiol 2009;587:2663-2676.
55. Mayer B, Brunner F, Schmidt K. Inhibition of nitric oxide synthesis by methylene blue. Biochem Pharmacol 1993;45:367-374.
56. Schrammel A, Behrends S, Schmidt K, Koesling D, Mayer B. Characterization of 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one as a heme-site inhibitor of nitric oxide-sensitive guanylyl cyclase. Mol Pharmacol 1996;50:1-5.
57. Guzman NJ, Fang MZ, Tang SS, Ingelfinger JR, Garg LC. Autocrine inhibition of Na+/K(+)-ATPase by nitric oxide in mouse proximal tubule epithelial cells. J Clin Invest 1995;95:2083-2088.
58. Lazrak A, Samanta A, Venetsanou K, Barbry P, Matalon S. Modification of biophysical properties of lung epithelial Na(+) channels by dexamethasone. Am J Physiol Cell Physiol 2000;279:C762-C770.
59. Kellenberger S, Gautschi I, Pfister Y, Schild L. Intracellular thiolmediated modulation of epithelial sodium channel activity. J Biol Chem 2005;280:7739-7747.
60. Wang S, Publicover S, Gu Y. An oxygen-sensitive mechanism in regulation of epithelial sodium channel. Proc Natl Acad Sci USA 2009;106:2957-2962.
61. Gupta S, McArthur C, Grady C, Ruderman NB. Stimulation of vascular Na(1)-K(+)-ATPase activity by nitric oxide: a cGMP-independent effect. Am J Physiol 1994;266:H2146-H2151.
62. William M, Vien J, Hamilton E, Garcia A, Bundgaard H, Clarke RJ, Rasmussen HH. The nitric oxide donor sodium nitroprusside stimulates the Na+-K+ pump in isolated rabbit cardiac myocytes. J Physiol 2005;565:815-825.
63. Varela M, Herrera M, Garvin JL. Inhibition of Na-K-ATPase in thick ascending limbs by NO depends on O2- and is diminished by a high-salt diet. Am J Physiol Renal Physiol 2004;287:F224-F230.
64. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 2005; 6:150-166.
65. Lazrak A, Iles KE, Liu G, Noah DL, Noah JW, Matalon S. Influenza virus M2 protein inhibits epithelial sodium channels by increasing reactive oxygen species. FASEB J 2009;23:3829-3842.
66. Song W, Liu G, Bosworth CA, Walker JR, Megaw GA, Lazrak A, Abraham E, Sullender WM, Matalon S. Respiratory syncytial virus inhibits lung epithelial Na+ channels by up-regulating inducible nitric-oxide synthase. J Biol Chem 2009;284:7294-7306.
67. Mehta S. The effects of nitric oxide in acute lung injury. Vascul Pharmacol 2005;43:390-403.