Alveolar nonselective channels are ASIC1a/α-ENaC channels and contribute to AFC

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 312, Issue 6, 2017, Pages L797-L811

  Trac, Phi T ^a   Thai, Tiffany L ^a   Linck, Valerie ^a   Zou, Li ^a   Greenlee, Megan ^a,d   Yue, Qiang ^a   Al Khalili, Otor ^a   Alli, Abdel A ^b   Eaton, Amity F ^a,c   Eaton, Douglas C ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d The American Physiological Society   (United States)

Author keywords

Acid sensing ion channel 1a; Alveolar fluid clearance; Alveoli; Lung fluid balance; Nonselective cation channels; epithelial Na+ channels

Indexed keywords

ACCN1 PROTEIN; ACCN2 PROTEIN; ACCN3 PROTEIN; ACCN5 PROTEIN; ACID SENSING ION CHANNEL; ACID SENSING ION CHANNEL 1A PROTEIN; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ALPHA EPITHELIAL SODIUM CHANNEL; EPITHELIAL SODIUM CHANNEL; PROTEIN; UNCLASSIFIED DRUG; OXYGEN; PROTEIN BINDING; PROTEIN SUBUNIT; SNAKE VENOM; WATER;

ALVEOLAR FLUID CLEARANCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; KNOCKOUT MOUSE; LUNG ALVEOLUS CELL TYPE 2; LUNG CLEARANCE; LUNG SLICE; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SUBUNIT; SINGLE CHANNEL PATCH CLAMP; SODIUM ABSORPTION; ANIMAL; BIOLOGICAL MODEL; BRONCHOALVEOLAR LAVAGE FLUID; C57BL MOUSE; CELL CULTURE; CHANNEL GATING; DRUG EFFECTS; LUNG ALVEOLUS; LUNG ALVEOLUS EPITHELIUM CELL; METABOLISM;

ACID SENSING ION CHANNELS; ALVEOLAR EPITHELIAL CELLS; ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CELLS, CULTURED; EPITHELIAL SODIUM CHANNELS; ION CHANNEL GATING; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; OXYGEN; PROTEIN BINDING; PROTEIN SUBUNITS; PULMONARY ALVEOLI; SNAKE VENOMS; WATER;

EID: 85020219879     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00379.2016     Document Type: Article

References (87)

1. Adir Y, Factor P, Dumasius V, Ridge KM, Sznajder JI. Na, K-ATPase gene transfer increases liquid clearance during ventilation-induced lung injury. Am J Respir Crit Care Med 168: 1445–1448, 2003. doi: 10.1164/ rccm.200207-702OC.
2. Alli AA, Bao HF, Alli AA, Aldrugh Y, Zhou Y, Yu L, Eaton DC. Calmodulin and CaM kinase II govern MARCKS-mediated PIP2-dependent regulation of ENaC. FASEB J 26, Suppl: 867-815, 2012.
3. Askwith CC, Benson CJ, Welsh MJ, Snyder PM. DEG/ENaC ion channels involved in sensory transduction are modulated by cold temperature. Proc Natl Acad Sci USA 98: 6459–6463, 2001. doi: 10.1073/pnas. 111155398.
4. Azzam ZS, Dumasius V, Saldias FJ, Adir Y, Sznajder JI, Factor P. Na, K-ATPase overexpression improves alveolar fluid clearance in a rat model of elevated left atrial pressure. Circulation 105: 497–501, 2002. doi: 10.1161/hc0402.102848.
5. Babinski K, Lê KT, Séguéla P. Molecular cloning and regional distribution of a human proton receptor subunit with biphasic functional properties. J Neurochem 72: 51–57, 1999. doi: 10.1046/j.1471-4159.1999. 0720051.x.
6. Bao HF, Liu L, Self J, Duke BJ, Ueno R, Eaton DC. A synthetic prostone activates apical chloride channels in A6 epithelial cells. Am J Physiol Gastrointest Liver Physiol 295: G234–G251, 2008. doi: 10.1152/ ajpgi.00366.2007.
7. Bao HF, Thai TL, Yue Q, Ma HP, Eaton AF, Cai H, Klein JD, Sands JM, Eaton DC. ENaC activity is increased in isolated, split-open cortical collecting ducts from protein kinase C+ knockout mice. Am J Physiol Renal Physiol 306: F309–F320, 2014. doi: 10.1152/ajprenal.00519.2013.
8. Barquin N, Ciccolella DE, Ridge KM, Sznajder JI. Dexamethasone upregulates the Na-K-ATPase in rat alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 273: L825–L830, 1997.
9. Bertog M, Cuffe JE, Pradervand S, Hummler E, Hartner A, Porst M, Hilgers KF, Rossier BC, Korbmacher C. Aldosterone responsiveness of the epithelial sodium channel (ENaC) in colon is increased in a mouse model for Liddle’s syndrome. J Physiol 586: 459–475, 2008. doi: 10.1113/ jphysiol.2007.140459.
10. +-ATPase motion and incorporation into the plasma membrane in response to G protein-coupled receptor signals in living cells. Mol Biol Cell 14: 1149-1157, 2003. doi: 10.1091/mbc.E02-06-0367.
11. Bohlen CJ, Chesler AT, Sharif-Naeini R, Medzihradszky KF, Zhou S, King D, Sánchez EE, Burlingame AL, Basbaum AI, Julius D. A heteromeric Texas coral snake toxin targets acid-sensing ion channels to produce pain. Nature 479: 410–414, 2011. doi: 10.1038/nature10607.
12. + channel in the collecting duct by vasopressin contributes to water reabsorption. Am J Physiol Renal Physiol 297: F1411–F1418, 2009. doi: 10. 1152/ajprenal.00371.2009.
13. Chen X, Kalbacher H, Gründer S. Interaction of acid-sensing ion channel (ASIC) 1 with the tarantula toxin psalmotoxin 1 is state dependent. J Gen Physiol 127: 267–276, 2006. doi: 10.1085/jgp.200509409.
14. Chen X, Kalbacher H, Gründer S. The tarantula toxin psalmotoxin 1 inhibits acid-sensing ion channel (ASIC) 1a by increasing its apparent H+ affinity. J Gen Physiol 126: 71–79, 2005. doi: 10.1085/jgp.200509303.
15. Chen XJ, Eaton DC, Jain L.-Adrenergic regulation of amiloridesensitive lung sodium channels. Am J Physiol Lung Cell Mol Physiol 282: L609–L620, 2002. doi: 10.1152/ajplung.00356.2001.
16. Chen XJ, Seth S, Yue G, Kamat P, Compans RW, Guidot D, Brown LA, Eaton DC, Jain L. Influenza virus inhibits ENaC and lung fluid clearance. Am J Physiol Lung Cell Mol Physiol 287: L366–L373, 2004. doi: 10.1152/ajplung.00011.2004.
17. Dada LA, Sznajder JI. Mechanisms of pulmonary edema clearance during acute hypoxemic respiratory failure: role of the Na, K-ATPase. Crit Care Med 31, Suppl: S248–S252, 2003. doi: 10.1097/01.CCM. 0000057895.22008.EC.
18. Davis IC, Matalon S. Epithelial sodium channels in the adult lung: important modulators of pulmonary health and disease. Adv Exp Med Biol 618: 127–140, 2007. doi: 10.1007/978-0-387-75434-5_10.
19. Dawson RJ, Benz J, Stohler P, Tetaz T, Joseph C, Huber S, Schmid G, Hügin D, Pflimlin P, Trube G, Rudolph MG, Hennig M, Ruf A. Structure of the acid-sensing ion channel 1 in complex with the gating modifier Psalmotoxin 1. Nat Commun 3: 936, 2012. doi: 10.1038/ ncomms1917.
20. Dobbs LG. Isolation and culture of alveolar type II cells. Am J Physiol Lung Cell Mol Physiol 258: L134–L147, 1990.
21. Dobbs LG, Gonzalez R, Williams MC. An improved method for isolating type II cells in high yield and purity. Am Rev Respir Dis 134: 141–145, 1986.
22. Downs CA, Kriener LH, Yu L, Eaton DC, Jain L, Helms MN.-Adrenergic agonists differentially regulate highly selective and nonselective epithelial sodium channels to promote alveolar fluid clearance in vivo. Am J Physiol Lung Cell Mol Physiol 302: L1167–L1178, 2012. doi: 10.1152/ajplung.00038.2012.
23. Eaton AF, Yue Q, Eaton DC, Bao HF. ENaC activity and expression is decreased in the lungs of protein kinase C-+ knockout mice. Am J Physiol Lung Cell Mol Physiol 307: L374–L385, 2014. doi: 10.1152/ajplung. 00040.2014.
24. Eaton DC. Intracellular sodium ion activity and sodium transport in rabbit urinary bladder. J Physiol 316: 527–544, 1981. doi: 10.1113/jphysiol.1981. sp013804.
25. Eaton DC, Becchetti A, Ma H, Ling BN. Renal sodium channels: regulation and single channel properties. Kidney Int 48: 941–949, 1995. doi: 10.1038/ki.1995.375.
26. + channels in lung alveolar type II epithelial cells. Proc Am Thorac Soc 1: 10–16, 2004. doi: 10.1513/pats.2306008.
27. Eaton DC, Helms MN, Koval M, Bao HF, Jain L. The contribution of epithelial sodium channels to alveolar function in health and disease. Annu Rev Physiol 71: 403–423, 2009. doi: 10.1146/annurev.physiol.010908. 163250.
28. Eaton DC, Marunaka Y, Ling BN. Ion channels in epithelial tissue: single-channel properties. In: Membrane Transport in Biology, edited by Schafer JA, Ussing HH, Kristensen P, and Giebisch GH. Berlin: Springer, 1992, p. 73–165. doi: 10.1007/978-3-642-76983-2_3.
29. Eaton DC, Ohara A, Ling BN, Marunaka Y, Duchatelle P, Kemendy AE, Kokko KE, Matsumoto PS, Hinton CF. Cellular regulation of amiloride-blockable sodium channels. Biomed Res 12, Suppl 2: 31–35, 1991.
30. Eaton DC, Trac P, Al Khalili OK, Greenlee MM. ASIC1a/+Enac hybrid channels contribute to alveolar fluid clearance (Abstract). Am J Respir Crit Care Med 193, Suppl: A5782, 2016.
31. +-ATPase 1 subunit gene improves alveolar fluid clearance and survival in hyperoxic rats. Hum Gene Ther 11: 2231–2242, 2000. doi: 10.1089/104303400750035753.
32. Flodby P, Kim YH, Beard LL, Gao D, Ji Y, Kage H, Liebler JM, Minoo P, Kim KJ, Borok Z, Crandall ED. Knockout mice reveal a major role for alveolar epithelial type I cells in alveolar fluid clearance. Am J Respir Cell Mol Biol 55: 395–406, 2016. doi: 10.1165/rcmb.2016-0005OC.
33. Fyfe GK, Canessa CM. Subunit composition determines the single channel kinetics of the epithelial sodium channel. J Gen Physiol 112: 423–432, 1998. doi: 10.1085/jgp.112.4.423.
34. García-Añoveros J, Derfler B, Neville-Golden J, Hyman BT, Corey DP. BNaC1 and BNaC2 constitute a new family of human neuronal sodium channels related to degenerins and epithelial sodium channels. Proc Natl Acad Sci USA 94: 1459–1464, 1997. doi: 10.1073/pnas.94.4. 1459.
35. Garty H, Palmer LG. Epithelial sodium channels: function, structure, and regulation. Physiol Rev 77: 359–396, 1997.
36. George AL Jr, Staub O, Geering K, Rossier BC, Kleyman TR, Kraehenbuhl JP. Functional expression of the amiloride-sensitive sodium channel in Xenopus oocytes. Proc Natl Acad Sci USA 86: 7295-7298, 1989. doi: 10.1073/pnas.86.18.7295.
37. Gille T, Randrianarison-Pellan N, Goolaerts A, Dard N, Uzunhan Y, Ferrary E, Hummler E, Clerici C, Planès C. Hypoxia-induced inhibition of epithelial Na (+) channels in the lung. Role of Nedd4-2 and the ubiquitin-proteasome pathway. Am J Respir Cell Mol Biol 50: 526–537, 2014. doi: 10.1165/rcmb.2012-0518OC.
38. Goldman DE. Potential, impedance, and rectification in membranes. J Gen Physiol 27: 37–60, 1943. doi: 10.1085/jgp.27.1.37.
39. Goodson P, Kumar A, Jain L, Kundu K, Murthy N, Koval M, Helms MN. Nadph oxidase regulates alveolar epithelial sodium channel activity and lung fluid balance in vivo via Oβ 2 signaling. Am J Physiol Lung Cell Mol Physiol 302: L410–L419, 2012. doi: 10.1152/ajplung.00260.2011.
40. Hardiman KM, McNicholas-Bevensee CM, Fortenberry J, Myles CT, Malik B, Eaton DC, Matalon S. Regulation of amiloride-sensitive Na (+) transport by basal nitric oxide. Am J Respir Cell Mol Biol 30: 720–728, 2004. doi: 10.1165/rcmb.2003-0325OC.
41. Helms MN, Chen XJ, Ramosevac S, Eaton DC, Jain L. Dopamine regulation of amiloride-sensitive sodium channels in lung cells. Am J Physiol Lung Cell Mol Physiol 290: L710–L722, 2006. doi: 10.1152/ ajplung.00486.2004.
42. Helms MN, Jain L, Self JL, Eaton DC. Redox regulation of epithelial sodium channels examined in alveolar type 1 and 2 cells patch-clamped in lung slice tissue. J Biol Chem 283: 22875–22883, 2008. doi: 10.1074/jbc. M801363200.
43. Helms MN, Self J, Bao HF, Job LC, Jain L, Eaton DC. Dopamine activates amiloride-sensitive sodium channels in alveolar type I cells in lung slice preparations. Am J Physiol Lung Cell Mol Physiol 291: L610-L618, 2006. doi: 10.1152/ajplung.00426.2005.
44. Hodgkin AL, Huxley AF, Katz B. Measurement of current-voltage relations in the membrane of the giant axon of Loligo. J Physiol 116: 424–448, 1952. doi: 10.1113/jphysiol.1952.sp004716.
45. Jacobson KA, Costanzi S, Joshi BV, Besada P, Shin DH, Ko H, Ivanov AA, Mamedova L. Agonists and antagonists for P2 receptors. Novartis Found Symp 276: 58–68, 2006. doi: 10.1002/9780470032244.ch6.
46. 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 Lung Cell Mol Physiol 274: L475–L484, 1998.
47. Jain L, Chen XJ, Malik B, Al-Khalili O, Eaton DC. Antisense oligonucleotides against the +-subunit of ENaC decrease lung epithelial cationchannel activity. Am J Physiol Lung Cell Mol Physiol 276: L1046–L1051, 1999.
48. Jain L, Chen XJ, Ramosevac S, Brown LA, 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.
49. Jain M, Sznajder JI. Effects of hypoxia on the alveolar epithelium. Proc Am Thorac Soc 2: 202–205, 2005. doi: 10.1513/pats.200501-006AC.
50. Johnson MD, Bao HF, Helms MN, Chen XJ, Tigue Z, Jain L, Dobbs LG, Eaton DC. 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: 4964–4969, 2006. doi: 10.1073/pnas.0600855103.
51. Kapoor N, Lee W, Clark E, Bartoszewski R, McNicholas CM, Latham CB, Bebok Z, Parpura V, Fuller CM, Palmer CA, Benos DJ. Interaction of ASIC1 and ENaC subunits in human glioma cells and rat astrocytes. Am J Physiol Cell Physiol 300: C1246–C1259, 2011. doi: 10.1152/ ajpcell.00199.2010.
52. + channels by ERK1/2 in chlorine-breathing mice. Am J Respir Cell Mol Biol 46: 342–354, 2012. doi: 10.1165/rcmb.2011-0309OC.
53. 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 23: 3829–3842, 2009. doi: 10.1096/fj.09-135590.
54. 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 278: L848–L857, 2000.
55. + channels by dexamethasone. Am J Physiol Cell Physiol 279: C762–C770, 2000.
56. Lewis SA, Diamond JM. Active sodium transport by mammalian urinary bladder. Nature 253: 747–748, 1975. doi: 10.1038/253747a0.
57. + transport by rabbit urinary bladder, a tight epithelium. J Membr Biol 28: 1–40, 1976. doi: 10.1007/BF01869689.
58. + transport by rabbit urinary bladder. J Membr Biol 28: 41–70, 1976. doi: 10.1007/ BF01869690.
59. Ma HP, Li L, Zhou ZH, Eaton DC, Warnock DG. ATP masks stretch activation of epithelial sodium channels in A6 distal nephron cells. Am J Physiol Renal Physiol 282: F501–F505, 2002. doi: 10.1152/ajprenal. 00147.2001.
60. +-permeant channels in the fetal distal lung epithelium. Pflugers Arch 431: 748–756, 1996. doi: 10.1007/BF02253839.
61. Marunaka Y, Tohda H, Hagiwara N, O’Brodovich H. Cytosolic Ca (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. doi: 10.1016/0006-291X (92) 91244-K.
62. McNicholas CM, Canessa CM. Diversity of channels generated by different combinations of epithelial sodium channel subunits. J Gen Physiol 109: 681–692, 1997. doi: 10.1085/jgp.109.6.681.
63. Mironova E, Bugay V, Pochynyuk O, Staruschenko A, Stockand JD. Recording ion channels in isolated, split-opened tubules. Methods Mol Biol 998: 341–353, 2013. doi: 10.1007/978-1-62703-351-0_27.
64. Nitta CH, Osmond DA, Herbert LM, Beasley BF, Resta TC, Walker BR, Jernigan NL. Role of ASIC1 in the development of chronic hypoxiainduced pulmonary hypertension. Am J Physiol Heart Circ Physiol 306: H41–H52, 2014. doi: 10.1152/ajpheart.00269.2013.
65. + and fluid absorption in the mammalian distal lung. Am J Physiol Lung Cell Mol Physiol 294: L401–L408, 2008. doi: 10.1152/ ajplung.00431.2007.
66. Planès C, Blot-Chabaud M, Matthay MA, Couette S, Uchida T, Clerici C. Hypoxia and 2-agonists regulate cell surface expression of the epithelial sodium channel in native alveolar epithelial cells. J Biol Chem 277: 47318–47324, 2002. doi: 10.1074/jbc.M209158200.
67. Planès C, Escoubet B, Blot-Chabaud M, Friedlander G, Farman N, Clerici C. Hypoxia downregulates expression and activity of epithelial sodium channels in rat alveolar epithelial cells. Am J Respir Cell Mol Biol 17: 508–518, 1997. doi: 10.1165/ajrcmb.17.4.2680.
68. Planès C, Randrianarison NH, Charles RP, Frateschi S, Cluzeaud F, Vuagniaux G, Soler P, Clerici C, Rossier BC, Hummler E. ENaCmediated alveolar fluid clearance and lung fluid balance depend on the channel-activating protease 1. EMBO Mol Med 2: 26–37, 2010. doi: 10. 1002/emmm.200900050.
69. Pochynyuk O, Bugaj V, Stockand JD. Physiologic regulation of the epithelial sodium channel by phosphatidylinositides. Curr Opin Nephrol Hypertens 17: 533–540, 2008. doi: 10.1097/MNH.0b013e328308fff3.
70. Pochynyuk O, Bugaj V, Vandewalle A, Stockand JD. Purinergic control of apical plasma membrane PI (4, 5) P2 levels sets ENaC activity in principal cells. Am J Physiol Renal Physiol 294: F38–F46, 2008. doi: 10.1152/ ajprenal.00403.2007.
71. Price MP, Gong H, Parsons MG, Kundert JR, Reznikov LR, Bernardinelli L, Chaloner K, Buchanan GF, Wemmie JA, Richerson GB, Cassell MD, Welsh MJ. Localization and behaviors in null mice suggest that ASIC1 and ASIC2 modulate responses to aversive stimuli. Genes Brain Behav 13: 179–194, 2014. doi: 10.1111/gbb.12108.
72. Rooj AK, McNicholas CM, Bartoszewski R, Bebok Z, Benos DJ, Fuller CM. Glioma-specific cation conductance regulates migration and cell cycle progression. J Biol Chem 287: 4053–4065, 2012. doi: 10.1074/ jbc.M111.311688.
73. Rossier BC, Canessa CM, Schild L, Horisberger JD. Epithelial sodium channels. Curr Opin Nephrol Hypertens 3: 487–496, 1994. doi: 10.1097/ 00041552-199409000-00003.
74. Rossier BC, Pradervand S, Schild L, Hummler E. Epithelial sodium channel and the control of sodium balance: interaction between genetic and environmental factors. Annu Rev Physiol 64: 877–897, 2002. doi: 10. 1146/annurev.physiol.64.082101.143243.
75. Staruschenko A, Patel P, Tong Q, Medina JL, Stockand JD. Ras activates the epithelial Na (+) channel through phosphoinositide 3-OH kinase signaling. J Biol Chem 279: 37771–37778, 2004. doi: 10.1074/jbc. M402176200.
76. + channel by phosphatidylinositide 3-OH kinase signaling in native collecting duct principal cells. J Am Soc Nephrol 18: 1652–1661, 2007. doi: 10.1681/ASN.2007010020.
77. + channel subunit proteins. J Biol Chem 275: 25760–25765, 2000. doi: 10.1074/jbc.M003615200.
78. Stockand JD, Mironova E, Bugaj V, Rieg T, Insel PA, Vallon V, Peti-Peterdi J, Pochynyuk O. Purinergic inhibition of ENaC produces aldosterone escape. J Am Soc Nephrol 21: 1903–1911, 2010. doi: 10.1681/ ASN.2010040377.
79. +-ATPase. J Appl Physiol (1985) 93: 1860–1866, 2002. doi: 10.1152/japplphysiol.00022.2002.
80. Urner M, Herrmann IK, Booy C, Roth-Z’ Graggen B, Maggiorini M, Beck-Schimmer B. Effect of hypoxia and dexamethasone on inflammation and ion transporter function in pulmonary cells. Clin Exp Immunol 169: 119–128, 2012. doi: 10.1111/j.1365-2249.2012.04595.x.
81. Wang S, Publicover S, Gu Y. An oxygen-sensitive mechanism in regulation of epithelial sodium channel. Proc Natl Acad Sci USA 106: 2957–2962, 2009. doi: 10.1073/pnas.0809100106.
82. + currents in intact fetal distal lung epithelial cells. Can J Physiol Pharmacol 71: 58–62, 1993. doi: 10.1139/y93-009.
83. Wemmie JA, Chen J, Askwith CC, Hruska-Hageman AM, Price MP, Nolan BC, Yoder PG, Lamani E, Hoshi T, Freeman JH Jr, Welsh MJ. The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron 34: 463–477, 2002. doi: 10.1016/S0896-6273 (02) 00661-X.
84. Wills NK, Lewis SA, Eaton DC. Active and passive properties of rabbit descending colon: a microelectrode and nystatin study. J Membr Biol 45: 81–108, 1979. doi: 10.1007/BF01869296.
85. Yu L, Cai H, Yue Q, Alli AA, Wang D, Al-Khalili O, Bao HF, Eaton DC. WNK4 inhibition of ENaC is independent of Nedd4-2-mediated ENaC ubiquitination. Am J Physiol Renal Physiol 305: F31–F41, 2013. doi: 10.1152/ajprenal.00652.2012.
86. Zhao M, Liang X, Ji H. Influenza infection impairs both ENaC and CFTR function in primary mouse tracheal epithelial cells. FASEB J 25, Suppl: 1042-18, 2011.
87. + channel. J Biol Chem 288: 5389–5397, 2013. doi: 10.1074/jbc.M112.425272.