Treatment of pulmonary edema by ENaC activators/stimulators

Current Molecular Pharmacology

Volumn 6, Issue 1, 2013, Pages 13-27

  Fronius, Martin ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Alveolar epithelium; ENaC; Fluid absorption; Lectin; Mineralo glucocorticoid; Proteolytic cleavage; adrenoceptor

Indexed keywords

APROTININ; BETA ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CYCLIC AMP DEPENDENT PROTEIN KINASE; EPITHELIAL SODIUM CHANNEL; EPITHELIAL SODIUM CHANNEL STIMULATING AGENT; GLUCOCORTICOID RECEPTOR; LECTIN; MINERALOCORTICOID RECEPTOR; PROTEINASE; PROTEINASE INHIBITOR; GLUCOCORTICOID; PEPTIDE HYDROLASE;

ADULT RESPIRATORY DISTRESS SYNDROME; ARTICLE; DNA FLANKING REGION; HEMORRHAGIC SHOCK; HUMAN; ION TRANSPORT; LECTIN BINDING; LUNG ALVEOLUS EPITHELIUM; LUNG EDEMA; LUNG FLUID; NONHUMAN; OSMOTIC PRESSURE; PRIORITY JOURNAL; PROTEIN DEGRADATION; RESPIRATORY FAILURE; SODIUM ABSORPTION; SODIUM TRANSPORT; CHEMISTRY; DRUG EFFECT; LUNG EXTRAVASCULAR FLUID; METABOLISM; PATHOLOGY; REVIEW; DRUG EFFECTS; PULMONARY EDEMA;

ADRENERGIC BETA-AGONISTS; EPITHELIAL SODIUM CHANNEL AGONISTS; EPITHELIAL SODIUM CHANNELS; EXTRAVASCULAR LUNG WATER; GLUCOCORTICOIDS; HUMANS; LECTINS; PEPTIDE HYDROLASES; PULMONARY EDEMA; RECEPTORS, ADRENERGIC, BETA;

EID: 84891622257     PISSN: 18744672     EISSN: 18744702     Source Type: Journal    
DOI: 10.2174/1874467211306010003     Document Type: Article

References (156)

1. Canessa, C.M. Structural biology: unexpected opening. Nature, 2007, 449, 293-294.
2. Canessa, C.M.; Schild, L.; Buell, G.; Thorens, B.; Gautschi, I.; Horisberger, J.D.; Rossier, B.C. Amiloride-sensitive epithelial Na+ channel is made of three homologous subunits. Nature, 1994, 367, 463-467.
3. Waldmann, R.; Champigny, G.; Bassilana, F.; Voilley, N.; Lazdunski, M. Molecular cloning and functional expression of a novel amiloride-sensitive Na+ channel. J BiolChem., 1995, 270, 27411-27414.
4. Giraldez, T.; Afonso-Oramas, D.; Cruz-Muros, I.; Garcia-Marin, V.; Pagel, P.; Gonzalez-Hernandez, T.; Alvarez de la Rosa, D. Cloning and functional expression of a new epithelial sodium channel delta subunit isoform differentially expressed in neurons of the human and monkey telencephalon. J. Neurochem., 2007, 102, 1304-1315.
5. Babini, E.; Geisler, H.S.; Siba, M.; Grunder, S. A new subunit of the epithelial Na+ channel identifies regions involved in Na+ selfinhibition. J. Biol.Chem., 2003, 278, 28418-28426.
6. Wesch, D.; Miranda, P.; Afonso-Oramas, D.; Althaus, M.; Castro- Hernandez, J.; Dominguez, J.; Morty, R.E.; Clauss, W.; Gonzalez- Hernandez, T.; Alvarez de la Rosa, D.; Giraldez, T. The neuronalspecific SGK1.1 kinase regulates {delta}-epithelial Na+ channel independently of PY motifs and couples it to phospholipase C signaling. Am. J. Physiol. Cell Physiol., 2010, 299, C779-C790.
7. Giraldez, T.; Rojas, P.; Jou, J.; Flores, C.; Alvarez de la Rosa, D. Invited Review- The epithelial sodium channel delta subunit: new notes for an old song. Am. J. Physiol. Renal Physiol., 2012, 303, F328-F338.
8. Lindemann, B.; Barbry, P.; Kretz, O.; Bock, R. Occurrence of ENaC subunit mRNA and immunocytochemistry of the channel subunits in taste buds of the rat vallate papilla. Ann. NY Acad. Sci., 1998, 855, 116-127.
9. Burch, L.H.; Talbot, C.R.; Knowles, M.R.; Canessa, C.M.; Rossier, B.C.; Boucher, R.C. Relative expression of the human epithelial Na+ channel subunits in normal and cystic fibrosis airways. Am. J. Physiol., 1995, 269, C511-C518.
10. Voilley, N.; Lingueglia, E.; Champigny, G.; Mattei, M.G.; Waldmann, R.; Lazdunski, M.; Barbry, P. The lung amiloride-sensitive Na+ channel: biophysical properties, pharmacology, ontogenesis, and molecular cloning. Proc. Natl. Acad. Sci. USA, 1994, 91, 247-251.
11. Olver, R.E.; Strang, L.B. Ion fluxes across the pulmonary epithelium and the secretion of lung liquid in the foetal lamb. J. Physiol., 1974, 241, 327-357.
12. Olver, R.E.; Walters, D.V.; M Wilson, S. Developmental regulation of lung liquid transport. Annu. Rev. Physiol., 2004, 66, 77-101.
13. Walters, D.V.; Olver, R.E. The role of catecholamines in lung liquid absorption at birth. Pediatr. Res., 1978, 12, 239-242.
14. Kleyman, T.R.; Cragoe, E.J.J. Amiloride and its analogs as tools in the study of ion transport. J. Membr. Biol., 1988, 105, 1-21.
15. Olver, R.E.; Ramsden, C.A.; Strang, L.B. Adrenaline-induced changes in net lung liquid volume flow across the pulmonary epi thelium of the fetal lamb: evidence for active sodium transport. J. Physiol., 1981, 319, 38P-53P.
16. Basset, G.; Crone, C.; Saumon, G. Significance of active ion transport in transalveolar water absorption: a study on isolated rat lung. J. Physiol., 1987, 384, 311-324.
17. Hummler, E.; Barker, P.; Gatzy, J.; Beermann, F.; Verdumo, C.; Schmidt, A.; Boucher, R.; Rossier, B.C. Early death due to defective neonatal lung liquid clearance in alpha-ENaC-deficient mice. Nat. Genet., 1996, 12, 325-328.
18. Bastacky, J.; Lee, C.Y.; Goerke, J.; Koushafar, H.; Yager, D.; Kenaga, L.; Speed, T.P.; Chen, Y.; Clements, J.A. Alveolar lining layer is thin and continuous: low-temperature scanning electron microscopy of rat lung. J. Appl. Physiol., 1995, 79, 1615-1628.
19. Ji, H.L.; Su, X.F.; Kedar, S.; Li, J.; Barbry, P.; Smith, P.R.; Matalon, S.; Benos, D.J. 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.
20. Jain, L.; Chen, X.J.; Ramosevac, S.; Brown, L.A.; Eaton, D.C. Expression of highly selective sodium channels in alveolar type II cells is determined by culture conditions. Am. J. Physiol. Lung Cell Mol. Physiol., 2001, 280, L646-658.
21. Matalon, S.; Lazrak, A.; Jain, L.; Eaton, D.C. Invited review: biophysical properties of sodium channels in lung alveolar epithelial cells. J. Appl. Physiol., 2002, 93, 1852-1859.
22. Althaus, M.; Clauss, W.G.; Fronius, M. Amiloride-sensitive sodium channels and pulmonary edema. Pulm. Med., 2011, 2011, 830320.
23. 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.
24. Ramminger, S.J.; Inglis, S.K.; Olver, R.E.; Wilson, S.M. Hormonal modulation of Na(+) transport in rat fetal distal lung epithelial cells. J. Physiol., 2002, 544, 567-577.
25. Clunes, M.T.; Butt, A.G.; Wilson, S.M. A glucocorticoid-induced Na+ conductance in human airway epithelial cells identified by perforated patch recording. J. Physiol., 2004, 557, 809-819.
26. Brown, S.G.; Gallacher, M.; Olver, R.E.; Wilson, S.M. 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.
27. Wilkinson, W.J.; Benjamin, A.R.; De Proost, I.; Orogo-Wenn, M.C.; Yamazaki, Y.; Staub, O.; Morita, T.; Adriaensen, D.; Riccardi, D.; Walters, D.V.; Kemp, P.J. Alveolar epithelial CNGA1 channels mediate cGMP-stimulated, amiloride-insensitive, lung liquid absorption. Pflugers Arch., 2011, 462, 267-279.
28. Junor, R.W.; Benjamin, A.R.; Alexandrou, D.; Guggino, S.E.; Walters, D.V. A novel role for cyclic nucleotide-gated cation channels in lung liquid homeostasis in sheep. J. Physiol., 1999, 520(Pt. 1), 255-260.
29. Staub, N.C. The pathogenesis of pulmonary edema. Prog. Cardiovasc. Dis., 1980, 23, 53-80.
30. Matthay, M.A.; Folkesson, H.G.; Clerici, C. Lung epithelial fluid transport and the resolution of pulmonary edema. Physiol. Rev., 2002, 82, 569-600.
31. Murray, J.F. Pulmonary edema: pathophysiology and diagnosis. Int. J. Tuberc. Lung Dis., 2011, 15, 155-160, i.
32. Simonneau, G.; Galie, N.; Rubin, L.J.; Langleben, D.; Seeger, W.; Domenighetti, G.; Gibbs, S.; Lebrec, D.; Speich, R.; Beghetti, M.; Rich, S.; Fishman, A. Clinical classification of pulmonary hypertension. J. Am. Coll. Cardiol., 2004, 43, 5S-12S.
33. Fronius, M.; Clauss, W.G.; Althaus, M. Why do we have to move fluid to be able to breathe? Front. Physiol., 2012, 3, 9.
34. Johnson, M.D.; Widdicombe, J.H.; Allen, L.; Barbry, P.; Dobbs, L.G. Alveolar epithelial type I cells contain transport proteins and transport sodium, supporting an active role for type I cells in regulation of lung liquid homeostasis. Proc. Natl. Acad. Sci. USA, 2002, 99, 1966-1971.
35. Johnson, M.D.; Bao, H.F.; Helms, M.N.; Chen, X.J.; Tigue, Z.; Jain, L.; Dobbs, L.G.; Eaton, D.C. Functional ion channels in pulmonary alveolar type I cells support a role for type I cells in lung ion transport. Proc. Natl. Acad. Sci. USA, 2006, 103, 4964-4969.
36. Benos, D.J.; Stanton, B.A. Functional domains within the degenerin/ epithelial sodium channel (Deg/ENaC) superfamily of ion channels. J. Physiol., 1999, 520(Pt. 3), 631-644.
37. Haerteis, S.; Krueger, B.; Korbmacher, C.; Rauh, R. The deltasubunit of the epithelial sodium channel (ENaC) enhances channel activity and alters proteolytic ENaC activation. J. Biol.Chem., 2009, 284, 29024-29040.
38. Freed, D.L.; Buckley, C.H. Mucotractive effect of lectin. Lancet, 1978, 1, 585-586.
39. Kunzelmann, K.; Sun, J.; Schreiber, R.; Konig, J. Effects of dietary lectinson ion transport in epithelia. Br. J. Pharmacol., 2004, 142, 1219-1226.
40. Yang, G.; Hamacher, J.; Gorshkov, B.; White, R.; Sridhar, S.; Verin, A.; Chakraborty, T.; Lucas, R. The Dual Role of TNF in Pulmonary Edema. J. Cardiovasc. Dis. Res.,2010, 1, 29-36.
41. Hazemi, P.; Tzotzos, S.J.; Fischer, B.; Andavan, G.S.; Fischer, H.; Pietschmann, H.; Lucas, R.; Lemmens-Gruber, R. Essential structural features of TNF-alpha lectin-like domain derived peptides for activation of amiloride-sensitive sodium current in A549 cells. J. Med. Chem., 2010, 53, 8021-8029.
42. Lucas, R.; Magez, S.; De Leys, R.; Fransen, L.; Scheerlinck, J.P.; Rampelberg, M.; Sablon, E.; De Baetselier, P. Mapping the lectinlike activity of tumor necrosis factor. Science, 1994, 263, 814-817.
43. Guice, K.S.; Oldham, K.T.; Remick, D.G.; Kunkel, S.L.; Ward, P.A. Anti-tumor necrosis factor antibody augments edema formation in caerulein-induced acute pancreatitis. J. Surg. Res., 1991, 51, 495-499.
44. Rezaiguia, S.; Garat, C.; Delclaux, C.; Meignan, M.; Fleury, J.; Legrand, P.; Matthay, M.A.; Jayr, C. Acute bacterial pneumonia in rats increases alveolar epithelial fluid clearance by a tumor necrosis factor-alpha-dependent mechanism. J. Clin. Invest., 1997, 99, 325-335.
45. Tillie-Leblond, I.; Guery, B.P.; Janin, A.; Leberre, R.; Just, N.; Pittet, J.F.; Tonnel, A.B.; Gosset, P. Chronic bronchial allergic inflammation increases alveolar liquid clearance by TNF-alpha - dependent mechanism. Am. J. Physiol. Lung Cell Mol. Physiol., 2002, 283, L1303-L1309.
46. Hribar, M.; Bloc, A.; van der Goot, F.G.; Fransen, L.; De Baetselier, P.; Grau, G.E.; Bluethmann, H.; Matthay, M.A.; Dunant, Y.; Pugin, J.; Lucas, R. The lectin-like domain of tumor necrosis factor-alpha increases membrane conductance in microvascular endothelial cells and peritoneal macrophages. Eur. J. Immunol., 1999, 29, 3105-3111.
47. Borjesson, A.; Norlin, A.; Wang, X.; Andersson, R.; Folkesson, H.G. TNF-alpha stimulates alveolar liquid clearance during intestinal ischemia-reperfusion in rats. Am. J. Physiol. Lung Cell Mol. Physiol., 2000, 278, L3-L12.
48. Fukuda, N.; Jayr, C.; Lazrak, A.; Wang, Y.; Lucas, R.; Matalon, S.; Matthay, M.A. Mechanisms of TNF-alpha stimulation of amiloride- sensitive sodium transport across alveolar epithelium. Am. J. Physiol. Lung Cell Mol. Physiol., 2001, 280, L1258-L1265.
49. Elia, N.; Tapponnier, M.; Matthay, M.A.; Hamacher, J.; Pache, J.C.; Brundler, M.A.; Totsch, M.; De Baetselier, P.; Fransen, L.; Fukuda, N.; Morel, D.R.; Lucas, R. Functional identification of the alveolar edema reabsorption activity of murine tumor necrosis factor- alpha. Am. J. Respir. Crit. Care Med., 2003, 168, 1043-1050.
50. Berthiaume, Y. Tumor necrosis factor and lung edema clearance: the tip of the iceberg? Am. J. Respir. Crit. Care Med., 2003, 168, 1022-1023.
51. Vadasz, I.; Schermuly, R.T.; Ghofrani, H.A.; Rummel, S.; Wehner, S.; Muhldorfer, I.; Schafer, K.P.; Seeger, W.; Morty, R.E.; Grimminger, F.; Weissmann, N. The lectin-like domain of tumor necrosis factor-alpha improves alveolar fluid balance in injured isolated rabbit lungs. Crit. Care Med., 2008, 36, 1543-1550.
52. Vallet, V.; Chraibi, A.; Gaeggeler, H.P.; Horisberger, J.D.; Rossier, B.C. An epithelial serine protease activates the amiloride-sensitive sodium channel. Nature, 1997, 389, 607-610.
53. Hughey, R.P.; Mueller, G.M.; Bruns, J.B.; Kinlough, C.L.; Poland, P.A.; Harkleroad, K.L.; Carattino, M.D.; Kleyman, T.R. Maturation of the epithelial Na+ channel involves proteolytic processing of the alpha- and gamma-subunits. J. Biol. Chem., 2003, 278, 37073-37082.
54. Caldwell, R.A.; Boucher, R.C.; Stutts, M.J. Serine protease activation of near-silent epithelial Na+ channels. Am. J. Physiol. Cell Physiol., 2004, 286, C190-C194.
55. Hughey, R.P.; Bruns, J.B.; Kinlough, C.L.; Harkleroad, K.L.; Tong, Q.; Carattino, M.D.; Johnson, J.P.; Stockand, J.D.; Kleyman, T.R. Epithelial sodium channels are activated by furin-dependent proteolysis. J. Biol. Chem., 2004, 279, 18111-18114.
56. Hughey, R.P.; Carattino, M.D.; Kleyman, T.R. Role of proteolysis in the activation of epithelial sodium channels. Curr. Opin. Nephrol. Hypertens., 2007, 16, 444-450.
57. Diakov, A.; Bera, K.; Mokrushina, M.; Krueger, B.; Korbmacher, C. Cleavage in the {gamma}-subunit of the epithelial sodium channel (ENaC) plays an important role in the proteolytic activation of near-silent channels. J. Physiol., 2008, 586, 4587-4608.
58. Vallet, V.; Pfister, C.; Loffing, J.; Rossier, B.C. Cell-surface expression of the channel activating protease xCAP-1 is required for activation of ENaC in the Xenopus oocyte. J. Am. Soc. Nephrol., 2002, 13, 588-594.
59. Rossier, B.C. The epithelial sodium channel: activation by membrane- bound serine proteases. Proc. Am. Thorac. Soc., 2004, 1, 4-9.
60. Bruns, J.B.; Carattino, M.D.; Sheng, S.; Maarouf, A.B.; Weisz, O.A.; Pilewski, J.M.; Hughey, R.P.; Kleyman, T.R. Epithelial Na+ channels are fully activated by furin- and prostasin-dependent release of an inhibitory peptide from the gamma-subunit. J. Biol. Chem., 2007, 282, 6153-6160.
61. Bridges, R.J.; Newton, B.B.; Pilewski, J.M.; Devor, D.C.; Poll, C.T.; Hall, R.L. Na+ transport in normal and CF human bronchial epithelial cells is inhibited by BAY 39-9437. Am. J. Physiol. Lung Cell Mol. Physiol., 2001, 281, L16-L23.
62. Tong, Z.; Illek, B.; Bhagwandin, V.J.; Verghese, G.M.; Caughey, G.H. Prostasin, a membrane-anchored serine peptidase, regulates sodium currents in JME/CF15 cells, a cystic fibrosis airway epithelial cell line. Am. J. Physiol. Lung Cell Mol. Physiol., 2004, 287, L928-L935.
63. Myerburg, M.M.; McKenna, E.E.; Luke, C.J.; Frizzell, R.A.; Kleyman, T.R.; Pilewski, J.M. Prostasin expression is regulated by airway surface liquid volume and is increased in cystic fibrosis. Am. J. Physiol. Lung Cell Mol. Physiol., 2008, 294, L932-L941.
64. Mall, M.; Bleich, M.; Greger, R.; Schreiber, R.; Kunzelmann, K. The amiloride-inhibitable Na+ conductance is reduced by the cystic fibrosis transmembrane conductance regulator in normal but not in cystic fibrosis airways. J. Clin. Invest., 1998, 102, 15-21.
65. Mall, M.; Grubb, B.R.; Harkema, J.R.; O'Neal, W.K.; Boucher, R.C. Increased airway epithelial Na+ absorption produces cystic fibrosis- like lung disease in mice. Nat. Med., 2004, 10, 487-493.
66. Verghese, G.M.; Tong, Z.Y.; Bhagwandin, V.; Caughey, G.H. Mouse prostasin gene structure, promoter analysis, and restricted expression in lung and kidney. Am. J. Respir. Cell Mol. Biol., 2004, 30, 519-529.
67. Planes, C.; Leyvraz, C.; Uchida, T.; Angelova, M.A.; Vuagniaux, G.; Hummler, E.; Matthay, M.; Clerici, C.; Rossier, B. In vitro and in vivo regulation of transepithelial lung alveolar sodium transport by serine proteases. Am. J. Physiol. Lung Cell Mol. Physiol.,2005, 288, L1099-L1109.
68. Planes, C.; Randrianarison, N.H.; Charles, R.P.; Frateschi, S.; Cluzeaud, F.; Vuagniaux, G.; Soler, P.; Clerici, C.; Rossier, B.C.; Hummler, E. ENaC-mediated alveolar fluid clearance and lung fluid balance depend on the channel-activating protease 1. EMBO Mol. Med., 2010, 2, 26-37.
69. Swystun, V.; Chen, L.; Factor, P.; Siroky, B.; Bell, P.D.; Matalon, S. Apical trypsin increases ion transport and resistance by a phospholipase C-dependent rise of Ca2+. Am. J. Physiol. Lung Cell Mol. Physiol., 2005, 288, L820-L830.
70. Lazrak, A.; Nita, I.; Subramaniyam, D.; Wei, S.; Song, W.; Ji, H.L.; Janciauskiene, S.; Matalon, S. Alpha(1)-antitrypsin inhibits epithelial Na+ transport in vitro and in vivo. Am. J. Respir. Cell Mol. Biol., 2009, 41, 261-270.
71. Garcia-Caballero, A.; Rasmussen, J.E.; Gaillard, E.; Watson, M.J.; Olsen, J.C.; Donaldson, S.H.; Stutts, M.J.; Tarran, R. SPLUNC1 regulates airway surface liquid volume by protecting ENaC from proteolytic cleavage. Proc. Natl. Acad. Sci. USA, 2009, 106, 11412-11417.
72. Bingle, C.D.; LeClair, E.E.; Havard, S.; Bingle, L.; Gillingham, P.; Craven, C.J. Phylogenetic and evolutionary analysis of the PLUNC gene family. Protein Sci.,2004, 13, 422-430.
73. Yamashima, T. JokichiTakamine (1854-1922), the samurai chemist, and his work on adrenalin. J. Med. Biogr., 2003, 11, 95-102.
74. Ahlquist, R.P. A study of the adrenotropic receptors. Am. J. Physiol., 1948, 153, 586-600.
75. Lefkowitz, R.J.; Hausdorff, W.P.; Caron, M.G. Role of phosphorylation in desensitization of the beta-adrenoceptor. Trends Pharmacol. Sci., 1990, 11, 190-194.
76. Olver, R.E.; Walters, D.V. The effect of catecholamines on foetal lung liquid secretion [proceedings]. J. Physiol.,1977, 273, 58P-59P.
77. Mason, R.J.; Williams, M.C.; Widdicombe, J.H.; Sanders, M.J.; Misfeldt, D.S.; Berry, L.C.J. Transepithelial transport by pulmonary alveolar type II cells in primary culture. Proc. Natl. Acad. Sci. USA, 1982, 79, 6033-6037.
78. Goodman, B.E.; Brown, S.E.; Crandall, E.D. Regulation of transport across pulmonary alveolar epithelial cell monolayers. J. Appl. Physiol., 1984, 57, 703-710.
79. Crandall, E.D.; Heming, T.A.; Palombo, R.L.; Goodman, B.E. Effects of terbutaline on sodium transport in isolated perfused rat lung. J. Appl. Physiol., 1986, 60, 289-294.
80. Berthiaume, Y.; Staub, N.C.; Matthay, M.A. Beta-adrenergic agonists increase lung liquid clearance in anesthetized sheep. J. Clin. Invest., 1987, 79, 335-343.
81. Pittet, J.F.; Wiener-Kronish, J.P.; McElroy, M.C.; Folkesson, H.G.; Matthay, M.A. Stimulation of lung epithelial liquid clearance by endogenous release of catecholamines in septic shock in anesthetized rats. J. Clin. Invest., 1994, 94, 663-671.
82. Casale, T.B.; Wood, D.; Wescott, S.; Kaliner, M. Immunohistochemical identification of lung cells responsive to beta-stimulation with a rise in cAMP. J Appl Physiol, 1987, 63, 434-439.
83. Hamid, Q.A.; Mak, J.C.; Sheppard, M.N.; Corrin, B.; Venter, J.C.; Barnes, P.J. Localization of beta 2-adrenoceptor messenger RNA in human and rat lung using in situ hybridization: correlation with receptor autoradiography. Eur. J. Pharmacol.,. 1991, 206, 133-138.
84. Mak, J.C.; Nishikawa, M.; Haddad, E.B.; Kwon, O.J.; Hirst, S.J.; Twort, C.H.; Barnes, P.J. Localisation and expression of betaadrenoceptor subtype mRNAs in human lung. Eur. J. Pharmacol., 1996, 302, 215-221.
85. Mutlu, G.M.; Dumasius, V.; Burhop, J.; McShane, P.J.; Meng, F.J.; Welch, L.; Dumasius, A.; Mohebahmadi, N.; Thakuria, G.; Hardiman, K.; Matalon, S.; Hollenberg, S.; Factor, P. Upregulation of alveolar epithelial active Na+ transport is dependent on beta2- adrenergic receptor signaling. Circ. Res., 2004, 94, 1091-1100.
86. Sakuma, T.; Tuchihara, C.; Ishigaki, M.; Osanai, K.; Nambu, Y.; Toga, H.; Takahashi, K.; Ohya, N.; Inoue, M.; Matthay, M.A. Beta1-adrenoceptor stimulation by high-dose terbutalinedownregulatesterbutaline- stimulated alveolar fluid clearance in ex vivo rat lung. Exp Lung Res, 2001, 27, 453-468.
87. Morgan, E.E.; Hodnichak, C.M.; Stader, S.M.; Maender, K.C.; Boja, J.W.; Folkesson, H.G.; Maron, M.B. Prolonged isoproterenol infusion impairs the ability of beta(2)-agonists to increase alveolar liquid clearance. Am. J. Physiol. Lung Cell Mol Physiol., 2002, 282, L666-L674.
88. Morgan, E.E.; Stader, S.M.; Hodnichak, C.M.; Mavrich, K.E.; Folkesson, H.G.; Maron, M.B. Postreceptor defects in alveolar epithelial beta-adrenergic signaling after prolonged isoproterenol infusion. Am. J. Physiol. Lung Cell Mol. Physiol., 2003, 285, L578-L583.
89. Maron, M.B.; Folkesson, H.G.; Stader, S.M.; Hodnichak, C.M. Impaired alveolar liquid clearance after 48-h isoproterenol infusion spontaneously recovers by 96 h of continuous infusion. Am. J. Physiol. Lung Cell Mol. Physiol., 2006, 291, L252-L256.
90. Saldias, F.; Lecuona, E.; Friedman, E.; Barnard, M.L.; Ridge, K.M.; Sznajder, J.I. Modulation of lung liquid clearance by isoproterenol in rat lungs. Am. J. Physiol., 1998, 274, L694-L701.
91. Dumasius, V.; Sznajder, J.I.; Azzam, Z.S.; Boja, J.; Mutlu, G.M.; Maron, M.B.; Factor, P. beta(2)-adrenergic receptor overexpression increases alveolar fluid clearance and responsiveness to endogenous catecholamines in rats. Circ. Res., 2001, 89, 907-914.
92. Minakata, Y.; Suzuki, S.; Grygorczyk, C.; Dagenais, A.; Berthiaume, Y. Impact of beta-adrenergic agonist on Na+ channel and Na+-K+-ATPase expression in alveolar type II cells. Am. J. Physiol., 1998, 275, L414-L422.
93. Thomas, C.P.; Campbell, J.R.; Wright, P.J.; Husted, R.F. cAMPstimulated Na+ transport in H441 distal lung epithelial cells: role of PKA, phosphatidylinositol 3-kinase, and sgk1. Am. J. Physiol. Lung Cell Mol. Physiol., 2004, 287, L843-L851.
94. Goodman, B.E.; Anderson, J.L.; Clemens, J.W. Evidence for regulation of sodium transport from airspace to vascular space by cAMP. Am. J. Physiol., 1989, 257, L86-L93.
95. Ito, Y.; Niisato, N.; O'Brodovich, H.; Marunaka, Y. The effect of brefeldin A on terbutaline-induced sodium absorption in fetal rat distal lung epithelium.Pflugers Arch., 1997, 434, 492-494.
96. Planes, C.; Blot-Chabaud, M.; Matthay, M.A.; Couette, S.; Uchida, T.; Clerici, C. Hypoxia and beta 2-agonists regulate cell surface expression of the epithelial sodium channel in native alveolar epithelial cells. J. Biol. Chem., 2002, 277, 47318-47324.
97. Bertorello, A.M.; Ridge, K.M.; Chibalin, A.V.; Katz, A.I.; Sznajder, J.I. Isoproterenol increases Na+-K+-ATPase activity by membrane insertion of alpha-subunits in lung alveolar cells. Am. J. Physiol., 1999, 276, L20-L27.
98. Kooijman, E.E.; Kuzenko, S.R.; Gong, D.; Best, M.D.; Folkesson, H.G. Phosphatidylinositol 4,5-bisphosphate stimulates alveolar epithelial fluid clearance in male and female adult rats. Am. J. Physiol. Lung Cell Mol. Physiol., 2011, 301, L804-L811.
99. Baloglu, E.; Ke, A.; Abu-Taha, I.H.; Bartsch, P.; Mairbaurl, H. In vitro hypoxia impairs beta2-adrenergic receptor signaling in primary rat alveolar epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol., 2009, 296, L500-L509.
100. Loeh, B.; Baloglu, E.; Ke, A.; Bartsch, P.; Mairbaurl, H. Beta2- adrenergic stimulation blunts inhibition of epithelial ion transport by hypoxia of rat alveolar epithelial cells. Cell Physiol. Biochem., 2010, 25, 123-134.
101. Modelska, K.; Matthay, M.A.; Brown, L.A.; Deutch, E.; Lu, L.N.; Pittet, J.F. Inhibition of beta-adrenergic-dependent alveolar epithelial clearance by oxidant mechanisms after hemorrhagic shock. Am. J. Physiol., 1999, 276, L844-L857.
102. Laffon, M.; Lu, L.N.; Modelska, K.; Matthay, M.A.; Pittet, J.F. alpha-adrenergic blockade restores normal fluid transport capacity of alveolar epithelium after hemorrhagic shock. Am. J. Physiol., 1999, 277, L760-L768.
103. Azzam, Z.S.; Saldias, F.J.; Comellas, A.; Ridge, K.M.; Rutschman, D.H.; Sznajder, J.I. Catecholamines increase lung edema clearance in rats with increased left atrial pressure. J. Appl. Physiol., 2001, 90, 1088-1094.
104. Sartori, C.; Allemann, Y.; Duplain, H.; Lepori, M.; Egli, M.; Lipp, E.; Hutter, D.; Turini, P.; Hugli, O.; Cook, S.; Nicod, P.; Scherrer, U. Salmeterol for the prevention of high-altitude pulmonary edema. N. Engl. J. Med., 2002, 346, 1631-1636.
105. Perkins, G.D.; McAuley, D.F.; Thickett, D.R.; Gao, F. The betaagonist lung injury trial (BALTI): a randomized placebo-controlled clinical trial. Am. J. Respir. Crit. Care Med., 2006, 173, 281-287.
106. Matthay, M.A.; Abraham, E. Beta-adrenergic agonist therapy as a potential treatment for acute lung injury. Am. J. Respir. Crit. Care Med., 2006, 173, 254-255.
107. Manocha, S.; Gordon, A.C.; Salehifar, E.; Groshaus, H.; Walley, K.R.; Russell, J.A. Inhaled beta-2 agonist salbutamol and acute lung injury: an association with improvement in acute lung injury. Crit. Care, 2006, 10, R12.
108. Licker, M.; Tschopp, J.M.; Robert, J.; Frey, J.G.; Diaper, J.; Ellenberger, C. Aerosolized salbutamol accelerates the resolution of pulmonary edema after lung resection. Chest, 2008, 133, 845-852.
109. Matthay, M.A.; Brower, R.G.; Carson, S.; Douglas, I.S.; Eisner, M.; Hite, D.; Holets, S.; Kallet, R.H.; Liu, K.D.; MacIntyre, N.; Moss, M.; Schoenfeld, D.; Steingrub, J.; Thompson, B.T. Randomized, placebo-controlled clinical trial of an aerosolized beta(2)- agonist for treatment of acute lung injury. Am. J. Respir. Crit. Care Med., 2011, 184, 561-568.
110. Gao Smith, F.; Perkins, G.D.; Gates, S.; Young, D.; McAuley, D.F.; Tunnicliffe, W.; Khan, Z.; Lamb, S.E. Effect of intravenous beta-2 agonist treatment on clinical outcomes in acute respiratory distress syndrome (BALTI-2): a multicentre, randomised controlled trial. Lancet, 2012, 379, 229-235.
111. Sartori, C.; Fang, X.; McGraw, D.W.; Koch, P.; Snider, M.E.; Folkesson, H.G.; Matthay, M.A. Selected contribution: long-term effects of beta(2)-adrenergic receptor stimulation on alveolar fluid clearance in mice. J. Appl. Physiol., 2002, 93, 1875-1880.
112. Ballard, P.L.; Baxter, J.D.; Higgins, S.J.; Rousseau, G.G.; Tomkins, G.M. General presence of glucocorticoid receptors in mammalian tissues. Endocrinology, 1974, 94, 998-1002.
113. Krozowski, Z.; Funder, J.W. Mineralocorticoid receptors in the rat lung.Endocrinology, 1981, 109, 1811-1813.
114. Fischer, H.; Clauss, W. Regulation of Na+ channels in frog lung epithelium: a target tissue for aldosterone action. Pflugers Arch., 1990, 416, 62-67.
115. Kunzelmann, K.; Kathofer, S.; Hipper, A.; Gruenert, D.C.; Gregner, R. Culture-dependent expression of Na+ conductances in airway epithelial cells. Pflugers Arch., 1996, 431, 578-586.
116. Suzuki, S.; Tsubochi, H.; Suzuki, T.; Darnel, A.D.; Krozowski, Z.S.; Sasano, H.; Kondo, T. Modulation of transalveolar fluid absorption by endogenous aldosterone in adult rats. Exp. Lung Res., 2001, 27, 143-155.
117. Keller-Wood, M.; von Reitzenstein, M.; McCartney, J. Is the fetal lung a mineralocorticoid receptor target organ? Induction of cortisol- regulated genes in the ovine fetal lung, kidney and small intestine. Neonatology, 2009, 95, 47-60.
118. Funder, J.W. Minireview: Aldosterone and mineralocorticoid receptors: past, present, and future. Endocrinology, 2010, 151, 5098-5102.
119. Morris, D.J.; Latif, S.A.; Brem, A.S. Interactions of mineralocorticoids and glucocorticoids in epithelial target tissues revisited. Steroids, 2009, 74, 1-6.
120. Barker, P.M.; Markiewicz, M.; Parker, K.A.; Walters, D.V.; Strang, L.B. Synergistic action of triiodothyronine and hydrocortisone on epinephrine-induced reabsorption of fetal lung liquid.Pediatr Res., 1990, 27, 588-591.
121. Champigny, G.; Voilley, N.; Lingueglia, E.; Friend, V.; Barbry, P.; Lazdunski, M. Regulation of expression of the lung amiloridesensitive Na+ channel by steroid hormones. EMBO J., 1994, 13, 2177-2181.
122. Tchepichev, S.; Ueda, J.; Canessa, C.; Rossier, B.C.; O'Brodovich, H. Lung epithelial Na channel subunits are differentially regulated during development and by steroids. Am. J. Physiol., 1995, 269, C805-C812.
123. Venkatesh, V.C.; Katzberg, H.D. Glucocorticoid regulation of epithelial sodium channel genes in human fetal lung. Am. J. Physiol., 1997, 273, L227-L233.
124. Renard, S.; Voilley, N.; Bassilana, F.; Lazdunski, M.; Barbry, P. Localization and regulation by steroids of the alpha, beta and gamma subunits of the amiloride-sensitive Na+ channel in colon, lung and kidney. Pflugers Arch., 1995, 430, 299-307.
125. Folkesson, H.G.; Norlin, A.; Wang, Y.; Abedinpour, P.; Matthay, M.A. Dexamethasone and thyroid hormone pretreatment upregulate alveolar epithelial fluid clearance in adult rats. J. Appl. Physiol., 2000, 88, 416-424.
126. Norlin, A.; Baines, D.L.; Folkesson, H.G. Role of endogenous cortisol in basal liquid clearance from distal air spaces in adult guinea-pigs. J. Physiol., 1999, 519(Pt. 1), 261-272.
127. Ramminger, S.J.; Richard, K.; Inglis, S.K.; Land, S.C.; Olver, R.E.; Wilson, S.M. A regulated apical Na(+) conductance in dexamethasone- treated H441 airway epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol., 2004, 287, L411-L419.
128. Richard, K.; Ramminger, S.J.; Forsyth, L.; Burchell, A.; Wilson, S.M. Thyroid hormone potentiates glucocorticoid-evoked airway Na+ transport without affecting alpha-ENaC transcription. FEBS Lett., 2004, 576, 339-342.
129. Althaus, M.; Pichl, A.; Clauss, W.G.; Seeger, W.; Fronius, M.; Morty, R.E. Nitric oxide inhibits highly selective sodium channels and the Na+/K+-ATPase in H441 cells. Am. J. Respir. Cell Mol. Biol., 2011, 44, 53-65.
130. Sayegh, R.; Auerbach, S.D.; Li, X.; Loftus, R.W.; Husted, R.F.; Stokes, J.B.; Thomas, C.P. Glucocorticoid induction of epithelial sodium channel expression in lung and renal epithelia occurs via trans-activation of a hormone response element in the 5'-flanking region of the human epithelial sodium channel alpha subunit gene. J. Biol. Chem., 1999, 274, 12431-12437.
131. Chow, Y.H.; Wang, Y.; Plumb, J.; O'Brodovich, H.; Hu, J. Hormonal regulation and genomic organization of the human amiloridesensitive epithelial sodium channel alpha subunit gene. Pediatr. Res., 1999, 46, 208-214.
132. Otulakowski, G.; Rafii, B.; Bremner, H.R.; O'Brodovich, H. Structure and hormone responsiveness of the gene encoding the alphasubunit of the rat amiloride-sensitive epithelial sodium channel. Am. J. Respir. Cell Mol. Biol., 1999, 20, 1028-1040.
133. Mick, V.E.; Itani, O.A.; Loftus, R.W.; Husted, R.F.; Schmidt, T.J.; Thomas, C.P. The alpha-subunit of the epithelial sodium channel is an aldosterone-induced transcript in mammalian collecting ducts, and this transcriptional response is mediated via distinct ciselements in the 5'-flanking region of the gene. Mol. Endocrinol., 2001, 15, 575-588.
134. Chen, S.Y.; Bhargava, A.; Mastroberardino, L.; Meijer, O.C.; Wang, J.; Buse, P.; Firestone, G.L.; Verrey, F.; Pearce, D. Epithelial sodium channel regulated by aldosterone-induced protein sgk. Proc. Natl. Acad. Sci. USA, 1999, 96, 2514-2519.
135. Alvarez de la Rosa, D.; Zhang, P.; Naray-Fejes-Toth, A.; Fejes- Toth, G.; Canessa, C.M. The serum and glucocorticoid kinase sgk increases the abundance of epithelial sodium channels in the plasma membrane of Xenopus oocytes. J. Biol. Chem., 1999, 274, 37834-37839.
136. Diakov, A.; Korbmacher, C. A novel pathway of epithelial sodium channel activation involves a serum- and glucocorticoid-inducible kinase consensus motif in the C terminus of the channel's alphasubunit. J. Biol. Chem., 2004, 279, 38134-38142.
137. Zhang, W.; Xia, X.; Reisenauer, M.R.; Rieg, T.; Lang, F.; Kuhl, D.; Vallon, V.; Kone, B.C. Aldosterone-induced Sgk1 relieves Dot1a- Af9-mediated transcriptional repression of epithelial Na+ channel alpha. J. Clin. Invest., 2007, 117, 773-783.
138. Itani, O.A.; Auerbach, S.D.; Husted, R.F.; Volk, K.A.; Ageloff, S.; Knepper, M.A.; Stokes, J.B.; Thomas, C.P. Glucocorticoidstimulated lung epithelial Na(+) transport is associated with regulated ENaC and sgk1 expression. Am. J. Physiol. Lung Cell Mol. Physiol., 2002, 282, L631-L641.
139. Itani, O.A.; Liu, K.Z.; Cornish, K.L.; Campbell, J.R.; Thomas, C.P. Glucocorticoids stimulate human sgk1 gene expression by activation of a GRE in its 5'-flanking region. Am. J. Physiol. Endocrinol. Metab., 2002, 283, E971-E979.
140. Dagenais, A.; Frechette, R.; Yamagata, Y.; Yamagata, T.; Carmel, J.F.; Clermont, M.E.; Brochiero, E.; Masse, C.; Berthiaume, Y. Downregulation of ENaC activity and expression by TNF-alpha in alveolar epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol., 2004, 286, L301-L311.
141. Dagenais, A.; Frechette, R.; Clermont, M.E.; Masse, C.; Prive, A.; Brochiero, E.; Berthiaume, Y. Dexamethasone inhibits the action of TNF on ENaC expression and activity. Am. J. Physiol. Lung Cell Mol. Physiol., 2006, 291, L1220-L1231.
142. Guney, S.; Schuler, A.; Ott, A.; Hoschele, S.; Zugel, S.; Baloglu, E.; Bartsch, P.; Mairbaurl, H. Dexamethasone prevents transport inhibition by hypoxia in rat lung and alveolar epithelial cells by stimulating activity and expression of Na+-K+-ATPase and epithelial Na+ channels. Am. J. Physiol. Lung Cell Mol. Physiol., 2007, 293, L1332-L1338.
143. Thompson, B.T. Corticosteroids for ARDS. Minerva Anestesiol., 2010, 76, 441-447.
144. Marik, P.E.; Meduri, G.U.; Rocco, P.R.; Annane, D. Glucocorticoid treatment in acute lung injury and acute respiratory distress syndrome.Crit. Care Clin., 2011, 27, 589-607.
145. Maggiorini, M.; Brunner-La Rocca, H.P.; Peth, S.; Fischler, M.; Bohm, T.; Bernheim, A.; Kiencke, S.; Bloch, K.E.; Dehnert, C.; Naeije, R.; Lehmann, T.; Bartsch, P.; Mairbaurl, H. Both tadalafil and dexamethasone may reduce the incidence of high-altitude pulmonary edema: a randomized trial. Ann. Intern. Med., 2006, 145, 497-506.
146. Fischler, M.; Maggiorini, M.; Dorschner, L.; Debrunner, J.; Bernheim, A.; Kiencke, S.; Mairbaurl, H.; Bloch, K.E.; Naeije, R.; Brunner-La Rocca, H.P. Dexamethasone but not tadalafil improves exercise capacity in adults prone to high-altitude pulmonary edema. Am. J. Respir. Crit. Care Med., 2009, 180, 346-352.
147. Kusche-Vihrog, K.; Sobczak, K.; Bangel, N.; Wilhelmi, M.; Nechyporuk-Zloy, V.; Schwab, A.; Schillers, H.; Oberleithner, H. Aldosterone and amiloride alter ENaC abundance in vascular endothelium. Pflugers Arch., 2008, 455, 849-857.
148. Oberleithner, H. Aldosterone makes human endothelium stiff and vulnerable. Kidney Int., 2005, 67, 1680-1682.
149. Oberleithner, H.; Riethmuller, C.; Schillers, H.; MacGregor, G.A.; de Wardener, H.E.; Hausberg, M. Plasma sodium stiffens vascular endothelium and reduces nitric oxide release. Proc. Natl. Acad. Sci. USA, 2007, 104, 16281-16286.
150. Fels, J.; Oberleithner, H.; Kusche-Vihrog, K. Menage a trois: aldosterone, sodium and nitric oxide in vascular endothelium. Biochim. Biophys. Acta, 2010, 1802, 1193-1202.
151. Maggiorini, M. Prevention and treatment of high-altitude pulmonary edema. Prog. Cardiovasc. Dis., 2010, 52, 500-506.
152. Matthay, M.A.; Wiener-Kronish, J.P. Intact epithelial barrier function is critical for the resolution of alveolar edema in humans. Am. Rev. Respir. Dis., 1990, 142, 1250-1257.
153. Ware, L.B.; Matthay, M.A. Alveolar fluid clearance is impaired in the majority of patients with acute lung injury and the acute respiratory distress syndrome. Am. J. Respir. Crit. Care Med., 2001, 163, 1376-1383.
154. Investigators, A.R.D.S.N. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network. N. Engl. J. Med., 2000, 342, 1301-1308.
155. Amasheh, S.; Milatz, S.; Krug, S.M.; Markov, A.G.; Gunzel, D.; Amasheh, M.; Fromm, M. Tight junction proteins as channel formers and barrier builders. Ann. NY Acad. Sci., 2009, 1165, 211-219.
156. Amasheh, S.; Milatz, S.; Krug, S.M.; Bergs, M.; Amasheh, M.; Schulzke, J.D.; Fromm, M. Na+ absorption defends from paracellular back-leakage by claudin-8 upregulation. Biochem. Biophys. Res. Commun., 2009, 378, 45-50.