Chloride transport-driven alveolar fluid secretion is a major contributor to cardiogenic lung edema

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 25, 2013, Pages

  Solymosi, Esther A ^a,b   Kaestle Gembardt, Stefanie M ^b   Vadász, István ^c   Wang, Liming ^a,d   Neye, Nils ^b   Chupin, Cécile Julie Adrienne ^a   Rozowsky, Simon ^a   Ruehl, Ramona ^c   Tabuchi, Arata ^a   Schulz, Holger ^e   Kapus, Andras ^a,f   Morty, Rory E ^f   Kuebler, Wolfgang M ^a,b,d,f,g  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

^d DEUTSCHES HERZZENTRUM BERLIN   (Germany)

^e INSTITUTE OF EPIDEMIOLOGY   (Germany)

^f UNIVERSITY OF TORONTO   (Canada)

^g MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

Author keywords

Epithelial Cl transport; Pulmonary edema

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AMILORIDE; CHLORIDE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL SODIUM CHANNEL; FUROSEMIDE; GLIBENCLAMIDE; OUABAIN; RADIOISOTOPE; SODIUM POTASSIUM CHLORIDE COTRANSPORTER;

ALVEOLAR FLUID SECRETION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHLORIDE TRANSPORT; DILUTION; HYDROSTATIC PRESSURE; LUNG ALVEOLUS; LUNG CLEARANCE; LUNG EDEMA; LUNG PERFUSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; SECRETION (PROCESS);

EPITHELIAL CL- TRANSPORT; PULMONARY EDEMA;

AMILORIDE; ANIMALS; BODY FLUIDS; CHLORIDES; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DIURETICS; FUROSEMIDE; HEART FAILURE; HYDROSTATIC PRESSURE; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED CFTR; PULMONARY ALVEOLI; PULMONARY EDEMA; RABBITS; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY MUCOSA; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SODIUM-POTASSIUM-EXCHANGING ATPASE;

MUS; STROPHANTHUS GRATUS;

EID: 84879286719     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1216382110     Document Type: Article

References (44)

1. Yin J, et al. (2008) Negative-feedback loop attenuates hydrostatic lung edema via a cGMP-dependent regulation of transient receptor potential vanilloid 4. Circ Res 102(8):966-974.
2. Kaestle SM, et al. (2007) Nitric oxide-dependent inhibition of alveolar fluid clearance in hydrostatic lung edema. Am J Physiol Lung Cell Mol Physiol 293(4):L859-L869.
3. Saldías FJ, et al. (2001) Alveolar fluid reabsorption is impaired by increased left atrial pressures in rats. Am J Physiol Lung Cell Mol Physiol 281(3):L591-L597.
4. Verghese GM, Ware LB, Matthay BA, Matthay MA (1999) Alveolar epithelial fluid transport and the resolution of clinically severe hydrostatic pulmonary edema. J Appl Physiol 87(4):1301-1312.
5. Matthay MA, Folkesson HG, Clerici C (2002) Lung epithelial fluid transport and the resolution of pulmonary edema. Physiol Rev 82(3):569-600.
6. Kuebler WM, et al. (2003) Stretch activates nitric oxide production in pulmonary vascular endothelial cells in situ. Am J Respir Crit Care Med 168(11):1391-1398.
7. Riordan JR (2005) Assembly of functional CFTR chloride channels. Annu Rev Physiol 67:701-718.
8. Lindert J, Perlman CE, Parthasarathi K, Bhattacharya J (2007) Chloride-dependent secretion of alveolar wall liquid determined by optical-sectioning microscopy. Am J Respir Cell Mol Biol 36(6):688-696.
9. + transport. Circ Res 96(9):999-1005.
10. Fang X, et al. (2006) Contribution of CFTR to apical-basolateral fluid transport in cultured human alveolar epithelial type II cells. Am J Physiol Lung Cell Mol Physiol 290(2):L242-L249.
11. Vadász I, et al. (2005) Oleic acid inhibits alveolar fluid reabsorption: A role in acute respiratory distress syndrome? Am J Respir Crit Care Med 171(5):469-479.
12. - transport across the air space-capillary barrier. J Appl Physiol 94(1):343-352.
13. Pickkers P, et al. (1997) Direct vascular effects of furosemide in humans. Circulation 96(6):1847-1852.
14. Johnson MD, et al. (2006) 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 103(13):4964-4969.
15. Ware LB, Matthay MA (2001) 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 163(6):1376-1383.
16. Folkesson HG, Matthay MA (2006) Alveolar epithelial ion and fluid transport: Recent progress. Am J Respir Cell Mol Biol 35(1):10-19.
17. Fang X, et al. (2002) Novel role for CFTR in fluid absorption from the distal airspaces of the lung. J Gen Physiol 119(2):199-207.
18. Dalemans W, et al. (1991) Altered chloride ion channel kinetics associated with the delta F508 cystic fibrosis mutation. Nature 354(6354):526-528.
19. French PJ, et al. (1995) Isotype-specific activation of cystic fibrosis transmembrane conductance regulator-chloride channels by cGMP-dependent protein kinase II. J Biol Chem 270(44):26626-26631.
20. Linsdell P (2001) Relationship between anion binding and anion permeability revealed by mutagenesis within the cystic fibrosis transmembrane conductance regulator chloride channel pore. J Physiol 531(Pt 1):51-66.
21. Nielsen VG, Duvall MD, Baird MS, Matalon S (1998) cAMP activation of chloride and fluid secretion across the rabbit alveolar epithelium. Am J Physiol 275(6 Pt 1):L1127-L1133.
22. - cotransporter in fetal rat alveolar type II pneumocyte. J Membr Biol 168(1):91-101.
23. Haas M, Forbush B, 3rd (2000) The Na-K-Cl cotransporter of secretory epithelia. Annu Rev Physiol 62:515-534.
24. Ali J, Chernicki W, Wood LD (1979) Effect of furosemide in canine low-pressure pulmonary edema. J Clin Invest 64(5):1494-1504.
25. Biddle TL, Yu PN (1979) Effect of furosemide on hemodynamics and lung water in acute pulmonary edema secondary to myocardial infarction. Am J Cardiol 43(1):86-90.
26. Ye X, Norlin A, Folkesson HG (2004) Stimulation of distal airspace fluid clearance in guinea pigs involves bumetanide-sensitive ion transport. Am J Obstet Gynecol 191(1):340-345.
27. Brumback AC, Staley KJ (2008) Thermodynamic regulation of NKCC1-mediated Clcotransport underlies plasticity of GABA (A) signaling in neonatal neurons. J Neurosci 28(6):1301-1312.
28. Donaldson SH, Poligone EG, Stutts MJ (2002) CFTR regulation of ENaC. Methods Mol Med 70:343-364.
29. Mall M, Grubb BR, Harkema JR, O'Neal WK, Boucher RC (2004) Increased airway epithelial Na+ absorption produces cystic fibrosis-like lung disease in mice. Nat Med 10(5):487-493.
30. Azad AK, et al. (2009) Mutations in the amiloride-sensitive epithelial sodium channel in patients with cystic fibrosis-like disease. Hum Mutat 30(7):1093-1103.
31. Jones GS, Miles PR, Lantz RC, Hinton DE, Castranova V (1982) Ionic content and regulation of cellular volume in rat alveolar type II cells. J Appl Physiol 53(1):258-266.
32. + conductance in adult alveolar pneumocytes. Am J Physiol 262(5 Pt 1):C1228-C1238.
33. Horisberger JD (2003) ENaC-CFTR interactions: The role of electrical coupling of ion fluxes explored in an epithelial cell model. Pflugers Arch 445(4):522-528.
34. O'Grady SM, Lee SY (2003) Chloride and potassium channel function in alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 284(5):L689-L700.
35. Pech V, et al. (2012) ENaC inhibition stimulates Cl-secretion in the mouse cortical collecting duct through an NKCC1-dependent mechanism. Am J Physiol Renal Physiol 303(1):F45-F55.
36. Bland RD, Nielson DW (1992) Developmental changes in lung epithelial ion transport and liquid movement. Annu Rev Physiol 54(1992):373-394.
37. Kounis NG, Nikolaou S, Zavras G, Siablis D (1986) Severe acute interstitial pulmonary edema from Moduretic (amiloride plus hydrochlorothiazide) . Ann Allergy 57(6):417-418.
38. Guo Y, DuVall MD, Crow JP, Matalon S (1998) Nitric oxide inhibits Na+ absorption across cultured alveolar type II monolayers. Am J Physiol 274(3 Pt 1):L369-L377.
39. Chen L, et al. (2008) DETANO and nitrated lipids increase chloride secretion across lung airway cells. Am J Respir Cell Mol Biol 39(2):150-162.
40. Ware LB, Matthay MA (2005) Clinical practice. Acute pulmonary edema. N Engl J Med 353(26):2788-2796.
41. Gray A, et al. (2008) Noninvasive ventilation in acute cardiogenic pulmonary edema. N Engl J Med 359(2):142-151.
42. Newton PJ, Davidson PM, Macdonald P, Ollerton R, Krum H (2008) Nebulized furosemide for the management of dyspnea: Does the evidence support its use? J Pain Symptom Manage 36(4):424-441.
43. Hoff RG, Rinkel GJ, Verweij BH, Algra A, Kalkman CJ (2010) Pulmonary edema and blood volume after aneurysmal subarachnoid hemorrhage: A prospective observational study. Crit Care 14(2):R43.
44. Grover RF, et al. (1998) β-adrenergic blockade does not prevent polycythemia or decrease in plasma volume in men at 4300 m altitude. Eur J Appl Physiol Occup Physiol 77(3):264-270.