A mutation of the epithelial sodium channel associated with atypical cystic fibrosis increases channel open probability and reduces Na+ self inhibition

Journal of Physiology

Volumn 588, Issue 8, 2010, Pages 1211-1225

  Rauh, Robert ^a   Diakov, Alexei ^a   Tzschoppe, Anja ^b   Korbmacher, Judit ^a   Azad, Abul Kalam ^c   Cuppens, Harry ^c   Cassiman, Jean Jaques ^c   Dötsch, Jörg ^b   Sticht, Heinrich ^a   Korbmacher, Christoph ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CHYMOTRYPSIN; CYSTEINE; EPITHELIAL SODIUM CHANNEL; GLUTAMIC ACID; SODIUM ION; TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL SODIUM CHANNEL ALPHA SUBUNIT; EPITHELIAL SODIUM CHANNEL BETA SUBUNIT; EPITHELIAL SODIUM CHANNEL GAMMA SUBUNIT; SODIUM; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CYSTIC FIBROSIS; GENE ACTIVITY; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENE MUTATION; HETEROZYGOSITY; NONHUMAN; OOCYTE; PHENOTYPE; PRIORITY JOURNAL; XENOPUS LAEVIS; ANIMAL CELL; CELL SURFACE; CHANNEL GATING; CONTROLLED STUDY; FEMALE; GAIN OF FUNCTION MUTATION; HETEROLOGOUS EXPRESSION; MUTATION; OUTSIDE OUT PATCH CLAMP; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; SINGLE CHANNEL PATCH CLAMP; SODIUM CURRENT;

ANIMALS; CELLS, CULTURED; CHYMOTRYPSIN; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL SODIUM CHANNEL; FEEDBACK, PHYSIOLOGICAL; FEMALE; HUMANS; MUTATION; OOCYTES; PATCH-CLAMP TECHNIQUES; PHENOTYPE; PLASMIDS; SODIUM; XENOPUS LAEVIS;

EID: 77953195725     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2009.180224     Document Type: Article

References (58)

1. Azad AK, Rauh R, Vermeulen F, Jaspers M, Korbmacher J, Boissier B. Mutations in the amiloride-sensitive epithelial sodium channel in patients with cystic fibrosis-like disease. Hum Mutat 2009, 30:1093-1103.
2. Boucher RC. New concepts of the pathogenesis of cystic fibrosis lung disease. Eur Respir J 2004, 23:146-158.
3. Boucher RC. Cystic fibrosis: a disease of vulnerability to airway surface dehydration. Trends Mol Med 2007, 13:231-240.
4. Bruns JB, Carattino MD, Sheng S, Maarouf AB, Weisz OA, Pilewski JM, Hughey RP, Kleyman TR. Epithelial Na+ channels are fully activated by furin- and prostasin-dependent release of an inhibitory peptide from theγ-subunit. J Biol Chem 2007, 282:6153-6160.
5. Caldwell RA, Boucher RC, Stutts MJ. Serine protease activation of near-silent epithelial Na+ channels. Am J Physiol Cell Physiol 2004, 286:C190-C194.
6. Caldwell RA, Boucher RC, Stutts MJ. Neutrophil elastase activates near-silent epithelial Na+ channels and increases airway epithelial Na+ transport. Am J Physiol Lung Cell Mol Physiol 2005, 288:L813-L819.
7. Canessa CM. Structural biology: unexpected opening. Nature 2007, 449:293-294.
8. Canessa CM, Schild L, Buell G, Thorens B, Gautschi I, Horisberger JD, Rossier BC. Amiloride-sensitive epithelial Na+ channel is made of three homologous subunits. Nature 1994, 367:463-467.
9. Carattino MD, Hughey RP, Kleyman TR. Proteolytic processing of the epithelial sodium channel γ subunit has a dominant role in channel activation. J Biol Chem 2008, 283:25290-25295.
10. Chraibi A, Horisberger JD. Na self inhibition of human epithelial Na channel: temperature dependence and effect of extracellular proteases. J Gen Physiol 2002, 120:133-145.
11. Chraibi A, Vallet V, Firsov D, Hess SK, Horisberger JD. Protease modulation of the activity of the epithelial sodium channel expressed in Xenopus oocytes. J Gen Physiol 1998, 111:127-138.
12. De Boeck K, Wilschanski M, Castellani C, Taylor C, Cuppens H, Dodge J, Sinaasappel M. Cystic fibrosis: terminology and diagnostic algorithms. Thorax 2006, 61:627-635.
13. Diakov A, Bera K, Mokrushina M, Krueger B, Korbmacher C. Cleavage in the γ-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.
14. 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 α-subunit. J Biol Chem 2004, 279:38134-38142.
15. Drummond GB. Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 2009, 587:713-719.
16. Durieux ME, Salafranca MN, Lynch KR. Trypsin induces Ca2+-activated Cl- currents in X. laevis oocytes. FEBS Lett 1994, 337:235-238.
17. Firsov D, Schild L, Gautschi I, Merillat AM, Schneeberger E, Rossier BC. Cell surface expression of the epithelial Na channel and a mutant causing Liddle syndrome: a quantitative approach. Proc Natl Acad Sci U S A 1996, 93:15370-15375.
18. Garty H, Palmer LG. Epithelial sodium channels: function, structure, and regulation. Physiol Rev 1997, 77:359-396.
19. Gonzales EB, Kawate T, Gouaux E. Pore architecture and ion sites in acid-sensing ion channels and P2X receptors. Nature 2009, 460:599-604.
20. Haerteis S, Krueger B, Korbmacher C, Rauh R. The δ-subunit of the epithelial sodium channel (ENaC) enhances channel activity and alters proteolytic ENaC activation. J Biol Chem 2009, 284:29024-29040.
21. Harris M, Firsov D, Vuagniaux G, Stutts MJ, Rossier BC. A novel neutrophil elastase inhibitor prevents elastase activation and surface cleavage of the epithelial sodium channel expressed in Xenopus laevis oocytes. J Biol Chem 2007, 282:58-64.
22. Huber R, Krueger B, Diakov A, Korbmacher J, Haerteis S, Einsiedel J. Functional characterization of a partial loss-of-function mutation of the epithelial sodium channel (ENaC) associated with atypical cystic fibrosis. Cell Physiol Biochem 2010, 25:145-158.
23. Hughey RP, Carattino MD, Kleyman TR. Role of proteolysis in the activation of epithelial sodium channels. Curr Opin Nephrol Hypertens 2007, 16:444-450.
24. Hummler E, Barker P, Gatzy J, Beermann F, Verdumo C, Schmidt A, Boucher R, Rossier BC. Early death due to defective neonatal lung liquid clearance in α-ENaC-deficient mice. Nat Genet 1996, 12:325-328.
25. Jasti J, Furukawa H, Gonzales EB, Gouaux E. Structure of acid-sensing ion channel 1 at 1.9 Å resolution and low pH. Nature 2007, 449:316-323.
26. Ji HL, Bishop LR, Anderson SJ, Fuller CM, Benos DJ. The role of Pre-H2 domains of α- and δ-epithelial Na+ channels in ion permeation, conductance, and amiloride sensitivity. J Biol Chem 2004, 279:8428-8440.
27. Kellenberger S, Gautschi I, Rossier BC, Schild L. Mutations causing Liddle syndrome reduce sodium-dependent downregulation of the epithelial sodium channel in the Xenopus oocyte expression system. J Clin Invest 1998, 101:2741-2750.
28. Kellenberger S, Schild L. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol Rev 2002, 82:735-767.
29. Kerem E, Bistritzer T, Hanukoglu A, Hofmann T, Zhou Z, Bennett W. Pulmonary epithelial sodium-channel dysfunction and excess airway liquid in pseudohypoaldosteronism. N Engl J Med 1999, 341:156-162.
30. Kleyman TR, Carattino MD, Hughey RP. ENaC at the cutting edge: regulation of the epithelial sodium channels by proteases. J Biol Chem 2009, 284:20447-20451.
31. Konstas AA, Bielfeld-Ackermann A, Korbmacher C. Sulfonylurea receptors inhibit the epithelial sodium channel (ENaC) by reducing surface expression. Pflugers Arch 2001, 442:752-761.
32. Konstas AA, Shearwin-Whyatt LM, Fotia AB, Degger B, Riccardi D, Cook DI, Korbmacher C, Kumar S. Regulation of the epithelial sodium channel by N4WBP5A, a novel Nedd4/Nedd4-2-interacting protein. J Biol Chem 2002, 277:29406-29416.
33. Korbmacher C, Volk T, Segal AS, Boulpaep EL, Fromter E. A calcium-activated and nucleotide-sensitive nonselective cation channel in M-1 mouse cortical collecting duct cells. J Membr Biol 1995, 146:29-45.
34. Kraus C, Reis A, Naehrlich L, Dötsch J, Korbmacher C, Rauh R. Functional characterization of a novel CFTR mutation P67S identified in a patient with atypical cystic fibrosis. Cell Physiol Biochem 2007, 19:239-248.
35. Mall M, Grubb BR, Harkema JR, O'Neal WK, Boucher RC. Increased airway epithelial Na+ absorption produces cystic fibrosis-like lung disease in mice. Nat Med 2004, 10:487-493.
36. Myerburg MM, Butterworth MB, McKenna EE, Peters KW, Frizzell RA, Kleyman TR, Pilewski JM. Airway surface liquid volume regulates ENaC by altering the serine protease-protease inhibitor balance: a mechanism for sodium hyperabsorption in cystic fibrosis. J Biol Chem 2006, 281:27942-27949.
37. Nesterov V, Dahlmann A, Bertog M, Korbmacher C. Trypsin can activate the epithelial sodium channel (ENaC) in microdissected mouse distal nephron. Am J Physiol Renal Physiol 2008, 295:F1052-F1062.
38. Randrianarison N, Escoubet B, Ferreira C, Fontayne A, Fowler-Jaeger N, Clerici C, Hummler E, Rossier BC, Planes C. β-Liddle mutation of the epithelial sodium channel increases alveolar fluid clearance and reduces the severity of hydrostatic pulmonary oedema in mice. J Physiol 2007, 582:777-788.
39. Rauh R, Dinudom A, Fotia AB, Paulides M, Kumar S, Korbmacher C, Cook DI. Stimulation of the epithelial sodium channel (ENaC) by the serum- and glucocorticoid-inducible kinase (Sgk) involves the PY motifs of the channel but is independent of sodium feedback inhibition. Pflugers Arch 2006, 452:290-299.
40. Rauh R, Korbmacher J, Cuppens H, Cassiman J-J, Korbmacher C. A heterozygous ENaC mutation (αW493R) identified in patients with atypical CF increases amiloride-sensitive currents in Xenopus laevis oocytes. Acta Physiol 2007, 192(Suppl 663):P08-L06-06.
41. Rauh R, Stuppy A, Diakov A, Korbmacher J, Azad AK, Doetsch J, Cuppens H, Cassiman J-J, Korbmacher C. Functional characterisation of a gain-of-function mutation of ENaC associated with atypical CF. Acta Physiol 2008, 192(Suppl 663):OM2-3-5.
42. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 1989, 245:1066-1073.
43. Rossier BC. Hormonal regulation of the epithelial sodium channel ENaC: N or Po?. J Gen Physiol 2002, 120:67-70.
44. Rossier BC, Schild L. Epithelial sodium channel: mendelian versus essential hypertension. Hypertension 2008, 52:595-600.
45. Rossier BC, Stutts MJ. Activation of the epithelial sodium channel (ENaC) by serine proteases. Annu Rev Physiol 2009, 71:361-379.
46. Schild L. The ENaC channel as the primary determinant of two human diseases: Liddle syndrome and pseudohypoaldosteronism. Nephrologie 1996, 17:395-400.
47. Schild L, Canessa CM, Shimkets RA, Gautschi I, Lifton RP, Rossier BC. A mutation in the epithelial sodium channel causing Liddle disease increases channel activity in the Xenopus laevis oocyte expression system. Proc Natl Acad Sci U S A 1995, 92:5699-5703.
48. Sheppard DN, Welsh MJ. Structure and function of the CFTR chloride channel. Physiol Rev 1999, 79:S23-S45.
49. Sheridan MB, Fong P, Groman JD, Conrad C, Flume P, Diaz R. Mutations in the β-subunit of the epithelial Na+ channel in patients with a cystic fibrosis-like syndrome. Hum Mol Genet 2005, 14:3493-3498.
50. Stanke F, Becker T, Cuppens H, Kumar V, Cassiman JJ, Jansen S. The TNFα receptor TNFRSF1A and genes encoding the amiloride-sensitive sodium channel ENaC as modulators in cystic fibrosis. Hum Genet 2006, 119:331-343.
51. Staub O, Verrey F. Impact of Nedd4 proteins and serum and glucocorticoid-induced kinases on epithelial Na+ transport in the distal nephron. J Am Soc Nephrol 2005, 16:3167-3174.
52. Stockand JD, Staruschenko A, Pochynyuk O, Booth RE, Silverthorn DU. Insight toward epithelial Na+ channel mechanism revealed by the acid-sensing ion channel 1 structure. IUBMB Life 2008, 60:620-628.
53. Tong Q, Menon AG, Stockand JD. Functional polymorphisms in the α-subunit of the human epithelial Na+ channel increase activity. Am J Physiol Renal Physiol 2006, 290:F821-F827.
54. Volk T, Konstas AA, Bassalay P, Ehmke H, Korbmacher C. Extracellular Na+ removal attenuates rundown of the epithelial Na+-channel (ENaC) by reducing the rate of channel retrieval. Pflugers Arch 2004, 447:884-894.
55. Waldmann R, Champigny G, Bassilana F, Voilley N, Lazdunski M. Molecular cloning and functional expression of a novel amiloride-sensitive Na+ channel. J Biol Chem 1995, 270:27411-27414.
56. Wielpütz MO, Lee IH, Dinudom A, Boulkroun S, Farman N, Cook DI, Korbmacher C, Rauh R. NDRG2 stimulates amiloride-sensitive Na+ currents in Xenopus laevis oocytes and Fisher rat thyroid cells. J Biol Chem 2007, 282:28264-28273.
57. Zerangue N, Schwappach B, Jan YN, Jan LY. A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane KATP channels. Neuron 1999, 22:537-548.
58. Zhou Z, Treis D, Schubert SC, Harm M, Schatterny J, Hirtz S, Duerr J, Boucher RC, Mall MA. Preventive but not late amiloride therapy reduces morbidity and mortality of lung disease in βENaC-overexpressing mice. Am J Respir Crit Care Med 2008, 178:1245-1256.