Functional characterization of a partial loss-of-function mutation of the epithelial sodium channel (ENaC) associated with atypical cystic fibrosis

Cellular Physiology and Biochemistry

Volumn 25, Issue 1, 2010, Pages 145-158

  Huber, Regina ^a   Krueger, Bettina ^a   Diakov, Alexei ^a   Korbmacher, Judit ^a   Haerteis, Silke ^a   Einsiedel, Jürgen ^b   Gmeiner, Peter ^b   Azad, Abul ^c   Cuppens, Harry ^c   Cassiman, Jean Jaques ^c   Korbmacher, Christoph ^a   Rauh, Robert ^a  

^a Inst Zellulare und Molec Physiol   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Electrophysiology; Heterologous expression; Ion channel; Xenopus laevis oocytes

Indexed keywords

CHYMOTRYPSIN; EPITHELIAL SODIUM CHANNEL; MUTANT PROTEIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL CELL; ARTICLE; CYSTIC FIBROSIS; FEMALE; HUMAN; LOSS OF FUNCTION MUTATION; NONHUMAN; OOCYTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; XENOPUS LAEVIS;

XENOPUS LAEVIS;

EID: 73849095120     PISSN: 10158987     EISSN: None     Source Type: Journal    
DOI: 10.1159/000272059     Document Type: Article

References (53)

1. 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.
2. Garty H, Palmer LG: Epithelial sodium channels: function, structure, and regulation. Physiol Rev 1997;77:359-396.
3. 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 alpha-ENaC-deficient mice. Nat Genet 1996;12:325-328.
4. Canessa CM: Structural biology: unexpected opening. Nature 2007;449:293-294.
5. Jasti J, Furukawa H, Gonzales EB, Gouaux E: Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature 2007;449:316-323.
6. + channel mechanism revealed by the acid-sensing ion channel 1 structure. IUBMB Life 2008;60:620-628.
7. 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.
8. Stanke F, Becker T, Cuppens H, Kumar V, Cassiman JJ, Jansen S, Radojkovic D, Siebert B, Yarden J, Ussery DW, Wienker TF, Tummler B: The TNFa receptor TNFRSF1A and genes encoding the amiloride-sensitive sodium channel ENaC as modulators in cystic fibrosis. Hum Genet 2006;119:331-343.
9. Boucher RC: New concepts of the pathogenesis of cystic fibrosis lung disease. Eur Respir J 2004;23:146-158.
10. Grubb BR, Boucher RC: Pathophysiology of gene-targeted mouse models for cystic fibrosis. Physiol Rev 1999;79:S193-214.
11. Snouwaert JN, Brigman KK, Latour AM, Malouf NN, Boucher RC, Smithies O, Koller BH: An animal model for cystic fibrosis made by gene targeting. Science 1992;257:1083-1088.
12. + absorption produces cystic fibrosis-like lung disease in mice. Nat Med 2004;10:487-493.
13. 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 bENaC-overexpressing mice. Am J Respir Crit Care Med 2008;178:1245-1256.
14. Chang SS, Grunder S, Hanukoglu A, Rosler A, Mathew PM, Hanukoglu I, Schild L, Lu Y, Shimkets RA, Nelson-Williams C, Rossier BC, Lifton RP: Mutations in subunits of the epithelial sodium channel cause salt wasting with hyperkalaemic acidosis, pseudohypoaldosteronism type 1. Nat Genet 1996;12:248-253.
15. Hanukoglu A, Bistritzer T, Rakover Y, Mandelberg A: Pseudohypoaldosteronism with increased sweat and saliva electrolyte values and frequent lower respiratory tract infections mimicking cystic fibrosis. J Pediatr 1994;125:752-755.
16. Marthinsen L, Kornfalt R, Aili M, Andersson D, Westgren U, Schaedel C: Recurrent Pseudomonas bronchopneumonia and other symptoms as in cystic fibrosis in a child with type I pseudohypoaldosteronism. Acta Paediatr 1998;87:472-474.
17. Schaedel C, Marthinsen L, Kristoffersson AC, Kornfalt R, Nilsson KO, Orlenius B, Holmberg L: Lung symptoms in pseudohypoaldosteronism type 1 are associated with deficiency of the alpha-subunit of the epithelial sodium channel. J Pediatr 1999;135:739-745.
18. + channel in patients with a cystic fibrosis-like syndrome. Hum Mol Genet 2005;14:3493-3498.
19. Kerem E, Bistritzer T, Hanukoglu A, Hofmann T, Zhou Z, Bennett W, MacLaughlin E, Barker P, Nash M, Quittell L, Boucher R, Knowles MR: Pulmonary epithelial sodium-channel dysfunction and excess airway liquid in pseudohypoaldosteronism. N Engl J Med 1999;341:156-162.
20. Cutting GR: Genetic heterogeneity and cystic fibrosis. Hum Mutat 2009;30:v.
21. Azad AK, Rauh R, Vermeulen F, Jaspers M, Korbmacher J, Boissier B, Bassinet L, Fichou Y, Georges MD, Stanke F, De Boeck K, Dupont L, Balascakova M, Hjelte L, Lebecque P, Radojkovic D, Castellani C, Schwartz M, Stuhrmann M, Schwarz M, Skalicka V, de Monestrol I, Girodon E, Ferec C, Claustres M, Tummler B, Cassiman JJ, Korbmacher C, Cuppens H: Mutations in the amiloride-sensitive epithelial sodium channel in patients with cystic fibrosis-like disease. Hum Mutat 2009;30:1093-1103.
22. 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.
23. + Currents in Xenopus laevis Oocytes and Fisher Rat Thyroid Cells. J Biol Chem 2007;282:28264-28273.
24. 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.
25. Diakov A, Bera K, Mokrushina M, Krueger B, Korbmacher C: Cleavage in the g-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.
26. 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 alpha-subunit. J Biol Chem 2004;279:38134-38142.
27. 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.
28. Zerangue N, Schwappach B, Jan YN, Jan LY: A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron 1999;22:537-548.
29. 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.
30. Lu M, Echeverri F, Kalabat D, Laita B, Dahan DS, Smith RD, Xu H, Staszewski L, Yamamoto J, Ling J, Hwang N, Kimmich R, Li P, Patron E, Keung W, Patron A, Moyer BD: Small molecule activator of the human epithelial sodium channel. J Biol Chem 2008;283:11981-11994.
31. 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.
32. 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.
33. + channel. J Biol Chem 1995;270:27411-27414.
34. + channel ENaC. J Physiol 2002;543:413-424.
35. Snyder PM, Bucher DB, Olson DR: Gating induces a conformational change in the outer vestibule of ENaC. J Gen Physiol 2000;116:781-790.
36. 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.
37. Kleyman TR, Myerburg MM, Hughey RP: Regulation of ENaCs by proteases: An increasingly complex story. Kidney Int 2006;70:1391-1392.
38. Kleyman TR, Carattino MD, Hughey RP: ENaC at the cutting edge: regulation of epithelial sodium channels by proteases. J Biol Chem. 2009;284:20447-20451
39. Rossier BC, Stutts MJ: Activation of the epithelial sodium channel (ENaC) by serine proteases. Annu Rev Physiol 2009;71:361-379.
40. - currents in X. laevis oocytes. FEBS Lett 1994;337:235-238.
41. Grunder S, Firsov D, Chang SS, Jaeger NF, Gautschi I, Schild L, Lifton RP, Rossier BC: A mutation causing pseudohypoaldosteronism type 1 identifies a conserved glycine that is involved in the gating of the epithelial sodium channel. EMBO J 1997;16:899-907.
42. + channel by peptidases. Curr Top Dev Biol 2007;78:23-46.
43. + 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.
44. Carattino MD, Passero CJ, Steren CA, Maarouf AB, Pilewski JM, Myerburg MM, Hughey RP, Kleyman TR: Defining an inhibitory domain in the alpha-subunit of the epithelial sodium channel. Am J Physiol Renal Physiol 2008;294:F47-52.
45. + channel is inhibited by a peptide derived from proteolytic processing of its alpha subunit. J Biol Chem 2006;281:18901-18907.
46. Carattino MD, Hughey RP, Kleyman TR: Proteolytic processing of the epithelial sodium channel gamma subunit has a dominant role in channel activation. J Biol Chem 2008;283:25290-25295.
47. Rossier BC: Hormonal regulation of the epithelial sodium channel ENaC: N or P(o)? J Gen Physiol 2002;120:67-70.
48. + channels. Am J Physiol Cell Physiol 2004;286:C190-194.
49. + transport. Am J Physiol Lung Cell Mol Physiol 2005;288:L813-819.
50. Bize V, Horisberger JD: Sodium self-inhibition of human epithelial sodium channel: selectivity and affinity of the extracellular sodium sensing site. Am J Physiol Renal Physiol 2007;293:F1137-1146.
51. Horisberger JD, Chraibi A: Epithelial sodium channel: a ligand-gated channel? Nephron Physiol 2004;96:p37-41.
52. Turnheim K: Intrinsic regulation of apical sodium entry in epithelia. Physiol Rev 1991;71:429-445.
53. + channel alpha subunit involved in gating. Pflugers Arch 1999;438:709-715.