Invited review: Biophysical properties of sodium channels in lung alveolar epithelial cells

Journal of Applied Physiology

Volumn 93, Issue 5, 2002, Pages 1852-1859

  Matalon, Sadis ^a   Lazrak, Ahmed ^a   Jain, Lucky ^a   Eaton, Douglas C ^a  

^a NONE

Author keywords

Alveolar type II cells; Amiloride sensitive epithelial sodium channels; ENaC; Lung sodium reabsorption

Indexed keywords

AMILORIDE; PROTEIN SUBUNIT; SODIUM CHANNEL;

ANIMAL CELL; FLUID BALANCE; LUNG ALVEOLUS EPITHELIUM; LUNG FLUID; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; REVIEW; SODIUM TRANSPORT; WATER TRANSPORT;

EID: 0036873397     PISSN: 87507587     EISSN: None     Source Type: Journal    
DOI: 10.1152/japplphysiol.01241.2001     Document Type: Review

References (91)

1. Barker PM, Gowen CW, Lawson EE, and Knowles MR. Decreased sodium ion absorption across nasal epithelium of very premature infants with respiratory distress syndrome. J Pediatr 130: 373-377, 1997.
2. Benos DJ. Amiloride: a molecular probe of sodium transport in tissues and cells. Am J Physiol Cell Physiol 242: C131-C145, 1982.
3. Berthiaume Y, Staub NC, and Matthay MA. Beta-adrenergic agonists increase lung liquid clearance in anesthetized sheep. J Clin Invest 79: 335-343, 1987.
4. Brignoni M, Pignataro OP, Rodriguez ML, Alvarez A, Vega-Salas DE, Rodriguez-Boulan E, and Salas PJ. Cyclic AMP modulates the rate of "constitutive" exocytosis of apical membrane proteins in Madin-Darby canine kidney cells. J Cell Sci 108: 1931-1943, 1995.
5. Butterworth MB, Helman SI, and Els WJ. cAMP-sensitive endocytic trafficking in A6 epithelia. Am J Physiol Cell Physiol 280: C752-C762, 2001.
6. Canessa CM, Horisberger JD, and Rossier BC. Epithelial sodium channel related to proteins involved in neurodegeneration. Nature 361: 467-470, 1993.
7. + channel is made of three homologous subunits. Nature 367: 463-467, 1994.
8. + channel from the epithelial cell line, A6. J Biol Chem 264: 20867-20870, 1989.
9. Carstairs JR, Nimmo AJ, and Barnes PJ. Autoradiographic visualization of beta-adrenoceptor subtypes in human lung. Am Rev Respir Dis 132: 541-547, 1985.
10. - secretion by arginine vasopressin in the amphibian cell line A6. Am J Physiol Cell Physiol 264: C1480-C1488, 1993.
11. Cheek JM, Kim KJ, and Crandall ED. Tight monolayers of rat alveolar epithelial cells: bioelectric properties and active sodium transport. Am J Physiol Cell Physiol 256: C688-C693, 1989.
12. Chen XJ, Eaton DC, and Jain L. β-Adrenergic regulation of amiloride-sensitive lung sodium channels. Am J Physiol Lung Cell Mol Physiol 282: L609-L620, 2002.
13. Crandall ED, Heming TA, Palombo RL, and Goodman BE. Effects of terbutaline on sodium transport in isolated perfused rat lung. J Appl Physiol 60: 289-294, 1986.
14. DeCoursey TE, Jacobs ER, and Silver MR. Potassium currents in rat type II alveolar epithelial cells. J Physiol 395: 487-505, 1988.
15. Ding C, Potter ED, Qiu W, Coon SL, Levine MA, and Guggino SE. Cloning and widespread distribution of the rat rod-type cyclic nucleotide-gated cation channel. Am J Physiol Cell Physiol 272: C1335-C1344, 1997.
16. Dobbs LG. Isolation and culture of alveolar type II cells. Am J Physiol Lung Cell Mol Physiol 258: L134-L147, 1990.
17. Eaton DC and Marunaka Y. Ion channel fluctuations: "noise" and single channel measurements. In: Current Topics in Membranes and Transport: Channels, Noise and Impedance in Epithelia, edited by Helman SI and Van Driessche W. New York: Academic, 1990.
18. Evans GJ, Wilkinson MC, Graham ME, Turner KM, Chamberlain LH, Burgoyne RD, and Morgan A. Phosphorylation of cysteine string protein by PKA: implications for the modulation of exocytosis. J Biol Chem 276: 47877-47885, 2001.
19. Factor P, Saldias F, Ridge K, Dumasius V, Zabner J, Jaffe HA, Blanco G, Barnard M, Mercer R, Perrin R, and Sznajder JI. Augmentation of lung liquid clearance via adenovirus-mediated transfer of a Na,K-ATPase β1 subunit gene. J Clin Invest 102: 1421-1430, 1998.
20. +-ATPase function in A549 cells. Am J Respir Cell Mol Biol 18: 741-749, 1998.
21. + channel along rat respiratory tract. Am J Physiol Cell Physiol 272: C131-C141, 1997.
22. Feng ZP, Clark RB, and Berthiaume Y. Identification of nonselective cation channels in cultured adult rat alveolar type II cells. Am J Respir Cell Mol Biol 9: 248-254, 1993.
23. Folkesson HG, Matthay MA, Hasegawa H, Kheradmand F, and Verkman AS. Transcellular water transport in lung alveolar epithelium through mercury-sensitive water channels. Proc Natl Acad Sci USA 91: 4970-4974, 1994.
24. Foster LJ, Yeung B, Mohtashami M, Ross K, Trimble WS, and Klip A. Binary interactions of the SNARE proteins syntaxin-4, SNAP23, and VAMP- 2 and their regulation by phosphorylation. Biochem J 37: 11089-11096, 1998.
25. + channels. FASEB J 8: 522-528, 1994.
26. Gowen CW Jr, Lawson EE, Gingras J, Boucher RC, Gatzy JT, and Knowles MR. Electrical potential difference and ion transport across nasal epithelium of term neonates: correlation with mode of delivery, transient tachypnea of the newborn, and respiratory rate. J Pediatr 113: 121-127, 1988.
27. Hamilton KL and Eaton DC. Single-channel recordings from amiloride-sensitive epithelial sodium channel. Am J Physiol Cell Physiol 249: C200-C207, 1985.
28. Hinton CF and Eaton DC. Expression of amiloride-blockable Na channels in Xenopus oocytes. Am J Physiol Cell Physiol 257: C825-C829, 1989.
29. Hummler E, Barker PM, Gatzy J, Beermann F, Verdumo C, Schmidt A, Boucher RC, and Rossier BC. Early death due to defective neonatal lung liquid clearance in α-ENaC-deficient mice. Nat Genet 12: 325-328, 1996.
30. Ito Y, Niisato N, O'Brodovich HM, and Marunaka Y. The effect of brefeldin A on terbutaline-induced sodium absorption in fetal rat distal lung epithelium. Pflügers Arch 434: 492-494, 1997.
31. Jain L, Chen XJ, Brown LA, and Eaton DC. Nitric oxide inhibits lung sodium transport through a cGMP-mediated inhibition of epithelial cation channels. Am J Physiol Lung Cell Mol Physiol 274: L475-L484, 1998.
32. Jain L, Chen XJ, Malik B, Al-Khalili OK, and Eaton DC. Antisense oligonucleotides against the α-subunit of ENaC decrease lung epithelial cation-channel activity. Am J Physiol Lung Cell Mol Physiol 276: L1046-L1051, 1999.
33. Jain L, Chen XJ, Ramosevac S, Brown LA, and Eaton DC. Expression of highly selective sodium channels in alveolar type II cells is determined by culture conditions. Am J Physiol Lung Cell Mol Physiol 280: L646-L658, 2001.
34. - channels. Am J Physiol Cell Physiol 275: C1610-C1620, 1998.
35. Katsura T, Gustafson CE, Ausiello DA, and Brown D. Protein kinase A phosphorylation is involved in regulated exocytosis of aquaporin-2 in transfected LLC-PK1 cells. Am J Physiol Renal Physiol 272: F817-F822, 1997.
36. Kemendy AE, Kleyman TR, and Eaton DC. Aldosterone alters the open probability of amiloride-blockable sodium channels in A6 epithelia. Am J Physiol Cell Physiol 263: C825-C837, 1992.
37. Kerem E, Bistritzer T, Hanukoglu A, Hofmann T, Zhou Z, Bennett W, MacLaughlin E, Barker P, Nash M, Quittell L, Boucher R, and Knowles MR. Pulmonary epithelial sodiumchannel dysfunction and excess airway liquid in pseudohypoaldosteronism. N Engl J Med 341: 156-162, 1999.
38. + channels in A6 cells. Am J Physiol Renal Fluid Electrolyte Physiol 266: F506-F511, 1994.
39. 2+ in pancreatic duct epithelial cells. J Gen Physiol 116: 507-520, 2000.
40. Lazrak A, Samanta A, and Matalon S. Biophysical properties and molecular characterization of amiloride-sensitive sodium channels in A549 cells. Am J Physiol Lung Cell Mol Physiol 278: L848-L857, 2000.
41. Light DB, McCann FV, Keller TM, and Stanton BA. Amiloride-sensitive cation channel in apical membrane of inner medullary collecting duct. Am J Physiol Renal Fluid Electrolyte Physiol 255: F278-F286, 1988.
42. + channels in A6 cells, a regulatory role for protein kinase C. Am J Physiol Renal Fluid Electrolyte Physiol 256: F1094-F1103, 1989.
43. Ling BN, Hinton CF, and Eaton DC. Potassium permeable channels in primary cultures of rabbit cortical collecting tubule. Kidney Int 40: 441-452, 1991.
44. Ling BN, Hinton CF, and Eaton DC. Amiloride-sensitive sodium channels in rabbit cortical collecting tubule primary cultures. Am J Physiol Renal Fluid Electrolyte Physiol 261: F933-F944, 1991.
45. + channel. A new channel type with homologies to Caenorhabditis elegans degenerins. FEBS Lett 318: 95-99, 1993.
46. + channels in fetal type II pneumocytes are regulated by G proteins. Am J Physiol Lung Cell Mol Physiol 267: L1-L8, 1994.
47. Machado JD, Morales A, Gomez JF, and Borges R. cAMP modulates exocytotic kinetics and increases quantal size in chromaffin cells. Mol Pharmacol 60: 514-520, 2001.
48. +-permeant channels in the fetal distal lung epithelium. Pflügers Arch 431:748-756, 1996.
49. Marunaka Y and Eaton DC. Effects of vasopressin and cAMP on single amiloride-blockable Na channels. Am J Physiol Cell Physiol 260: C1071-C1084, 1991.
50. - in fetal rat alveolar epithelium. J Physiol 515: 669-683, 1999.
51. 2+-induced modulation of ion selectivity and amiloride sensitivity of a cation channel and beta agonist action in fetal lung epithelium. Biochem Biophys Res Commun 187: 648-656, 1992.
52. + channels. Am J Physiol Lung Cell Mol Physiol 264: L357-L364, 1993.
53. + channels in alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 271: L1-L22, 1996.
54. + conductance in adult alveolar pneumocytes. Am J Physiol Cell Physiol 262: C1228-C1238, 1992.
55. Matalon S and O'Brodovich HM. Sodium channels in alveolar epithelial cells: molecular characterization, biophysical properties, and physiological significance. Annu Rev Physiol 61: 627-661, 1999.
56. Matthay MA, Folkesson HG, and Clerici C. Epithelial fluid transport and the resolution of pulmonary edema. Physiol Rev 82: 569-600, 2002.
57. Matthay MA, Folkesson HG, and Verkman AS. Salt and water transport across alveolar and distal airway epithelia in the adult lung. Am J Physiol Lung Cell Mol Physiol 270: L487-L503, 1996.
58. Matthay MA and Wiener-Kronish JP. Intact epithelial barrier function is critical for the resolution of alveolar edema in humans. Am Rev Respir Dis 142: 1250-1257, 1990.
59. - in rat fetal distal lung epithelium. Am J Physiol Cell Physiol 269: C156-C162, 1995.
60. Nielsen VG, Duvall MD, Baird MS, and Matalon S. cAMP activation of chloride and fluid secretion across the rabbit alveolar epithelium. Am J Physiol Lung Cell Mol Physiol 275: L1127-L1133, 1998.
61. Nielson DW and Lewis MB. Effects of amiloride on alveolar epithelial PD and fluid composition in rabbits. Am J Physiol Lung Cell Mol Physiol 258: L215-L219, 1990.
62. 2+ release from intracellular stores. Can J Physiol Pharmacol 75: 1030-1033, 1997.
63. + channel in the developing rat lung. Am J Physiol Cell Physiol 265: C491- C496, 1993.
64. O'Brodovich HM, Hannam V, Seear M, and Mullen JB. Amiloride impairs lung water clearance in newborn guinea pigs. J Appl Physiol 68: 1758-1762, 1990.
65. + channel in planar lipid bilayers. Am J Physiol Cell Physiol 264: C1489-C1499, 1993.
66. Ohara A, Matsunaga H, and Eaton DC. G protein activation inhibits amiloride-blockable highly selective sodium channels in A6 cells. Am J Physiol Cell Physiol 264: C352-C360, 1993.
67. Orser BA, Bertlik M, Fedorko L, and O'Brodovich HM. Cation selective channel in fetal alveolar type II epithelium. Biochim Biophys Acta 1094: 19-26, 1991.
68. Palmer LG. Epithelial Na channels: function and diversity. Annu Rev Physiol 54: 51-66, 1992.
69. Palmer LG and Frindt G. Amiloride-sensitive Na channels from the apical membrane of the rat cortical collecting tubule. Proc Natl Acad Sci USA 83: 2767-2770, 1986.
70. + pump modulation. Am J Physiol Renal Fluid Electrolyte Physiol 246: F517-F525, 1984.
71. Renard S, Voilley N, Bassilana F, Lazdunski M, and Barbry P. Localization and regulation by steroids of the α-, β-, and γ-subunits of the amiloride-sensitive Na channel in colon, lung, and kidney. Pflügers Arch 430: 299-307, 1995.
72. + channel (α rENaC) mediates its localization at the apical membrane. EMBO J 13: 4440-4450, 1994.
73. Ruddy MK, Drazen JM, Pitkanen OM, Rafii B, O'Brodovich HM, and Harris HW Jr. Modulation of aquaporin 4 and the amiloride-inhibitable sodium channel in perinatal rat lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 274: L1066-L1072, 1998.
74. + channel subunit that binds amiloride. Am J Physiol Cell Physiol 263: C1111- C1117, 1992.
75. Schwiebert EM, Potter ED, Hwang TH, Woo JS, Ding C, Qiu Guggino WB, Levine MA, and Guggino SE. cGMP stimulates sodium and chloride currents in rat tracheal airway epithelia. Am J Physiol Cell Physiol 272: C911-C922, 1997.
76. + channel protein into planar lipid bilayers. Am J Physiol Cell Physiol 268: C1148-C1156, 1995.
77. + channel (ENaC) expression in the developing normal and abnormal human perinatal lung. Am J Respir Crit Care Med 161: 1322-1331, 2000.
78. Smith PR, Saccomani G, Joe EH, Angelides KJ, and Benos DJ. Amiloride-sensitive sodium channel is linked to the cytoskeleton in renal epithelial cells. Proc Natl Acad Sci USA 88: 6971-6975, 1991.
79. Snyder PM, Cheng C, Prince LS, Rogers JC, and Welsh MJ. Electrophysiological and biochemical evidence that DEG/ ENaC cation channels are composed of nine subunits. J Biol Chem 273: 681-684, 1998.
80. Talbot CL, Bosworth DG, Briley EL, Fenstermacher DA, Boucher RC, Gabriel SE, and Barker PM. Quantitation and localization of ENaC subunit expression in fetal, newborn, and adult mouse lung. Am J Respir Cell Mol Biol 20: 398-406, 1999.
81. Talbot CL, Bosworth DG, Briley EL, Fenstermacher DA, Boucher RC, Gabriel SE, and Barker PM. Quantitation and localization of ENaC subunit expression in fetal, newborn, and adult mouse lung. Am J Respir Cell Mol Biol 20: 398-406, 1999.
82. Tchepichev S, Ueda J, Canessa CM, Rossier BC, and O'Brodovich HM. Lung epithelial Na channel subunits are differentially regulated during development and by steroids. Am J Physiol Cell Physiol 269: C805-C812, 1995.
83. + in nanoliter samples using chromogenic macrocyclic ionophores. Am J Physiol Renal Fluid Electrolyte Physiol 257: F893-F898, 1989.
84. 2+-activated nonselective cation channel in β-agonist-treated fetal distal lung epithelium. Am J Physiol Cell Physiol 266: C104-C109, 1994.
85. Verkman AS, Matthay MA, and Song Y. Aquaporin water channels and lung physiology. Am J Physiol Lung Cell Mol Physiol 278: L867-L879, 2000.
86. Verrey F, Groscurth P, and Bolliger U. Cytoskeletal disruption in A6 kidney cells: impact on endo/exocytosis and NaCl transport regulation by antidiuretic hormone. J Membr Biol 145: 193-204, 1995.
87. + channel: biophysical properties, pharmacology, ontogenesis, and molecular cloning. Proc Natl Acad Sci USA 91: 247-251, 1994.
88. Ware LB and Matthay MA. 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: 1376-1383, 2001.
89. Yue G and Matalon S. Mechanisms and sequelae of increased alveolar fluid clearance in hyperoxic rats. Am J Physiol Lung Cell Mol Physiol 272: L407-L412, 1997.
90. Yue G, Russell WJ, Benos DJ, Jackson RM, Olman MA, and Matalon S. Increased expression and activity of sodium channels in alveolar type II cells of hyperoxic rats. Proc Natl Acad Sci USA 92: 8418-8422, 1995.
91. Yue G, Shoemaker RL, and Matalon S. Regulation of low-amiloride-affinity sodium channels in alveolar type II cells. Am J Physiol Lung Cell Mol Physiol 267: L94-L100, 1994.