Aldosterone responsiveness of the epithelial sodium channel (ENaC) in colon is increased in a mouse model for Liddle's syndrome

Journal of Physiology

Volumn 586, Issue 2, 2008, Pages 459-475

  Bertog, Marko ^a,c   Cuffe, John E ^c   Pradervand, Sylvain ^d   Hummler, Edith ^d   Hartner, Andrea ^b   Porst, Markus ^b   Hilgers, Karl F ^b   Rossier, Bernard C ^d   Korbmacher, Christoph ^a,c  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ALDOSTERONE; AMILORIDE; EPITHELIAL SODIUM CHANNEL ALPHA SUBUNIT; EPITHELIAL SODIUM CHANNEL BETA SUBUNIT; EPITHELIAL SODIUM CHANNEL GAMMA SUBUNIT; ION CHANNEL; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; SODIUM CHANNEL; UNCLASSIFIED DRUG; EPITHELIAL SODIUM CHANNEL; SODIUM ION;

ALDOSTERONE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLON ABSORPTION; COLON MUCOSA; CONTROLLED STUDY; DESCENDING COLON; EX VIVO STUDY; FEEDBACK SYSTEM; FEMALE; LIDDLE SYNDROME; MALE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SALT INTAKE; SHORT CIRCUIT CURRENT; SODIUM TRANSPORT; UPREGULATION; WILD TYPE; HORMONE RESPONSE; IN VITRO STUDY; PROTEIN FUNCTION; SODIUM RESTRICTION; TISSUE SECTION; TRANSCRIPTION REGULATION;

ALDOSTERONE; ANIMALS; COLON; DISEASE MODELS, ANIMAL; EPITHELIAL SODIUM CHANNEL; FEMALE; HYPERTENSION; HYPOKALEMIA; IMMEDIATE-EARLY PROTEINS; KIDNEY; LUNG; MALE; MICE; MICE, MUTANT STRAINS; PROTEIN-SERINE-THREONINE KINASES; RENIN; SODIUM, DIETARY; SYNDROME;

EID: 38149123365     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2007.140459     Document Type: Article

References (59)

1. Abriel H & Horisberger JD (1999). Feedback inhibition of rat amiloride-sensitive epithelial sodium channels expressed in Xenopus laevis oocytes. J Physiol 516, 31-43.
2. Amasheh S, Barmeyer C, Koch CS, Tavalali S, Mankertz J, Epple HJ, Gehring MM, Florian P, Kroesen AJ, Zeitz M, Fromm M & Schulzke JD (2004). Cytokine-dependent transcriptional down-regulation of epithelial sodium channel in ulcerative colitis. Gastroenterology 126, 1711-1720.
3. Anantharam A, Tian Y & Palmer LG (2006). Open probability of the epithelial sodium channel is regulated by intracellular sodium. J Physiol 574, 333-347.
4. + channel subunits. Am J Physiol Cell Physiol 271, C605-C611.
5. + channel mutants causing Liddle's syndrome retain ability to respond to aldosterone and vasopressin. Am J Physiol Renal Physiol 285, F459-F471.
6. + absorption is preserved in a mouse model for Liddle's syndrome. Pflugers Arch 447 (Suppl.), S120.
7. Bertog M, Letz B, Kong W, Steinhoff M, Higgins MA, Bielfeld Ackermann A, Fromter E, Bunnett NW & Korbmacher C (1999). Basolateral proteinase-activated receptor (PAR-2) induces chloride secretion in M-1 mouse renal cortical collecting duct cells. J Physiol 521, 3-17.
8. Bertog M, Pradervand S, Hummler E, Rossier BC & Korbmacher C (2006). Sodium feedback regulation is partially preserved in a mouse model for Liddle's syndrome. Acta Physiol 186 (Suppl. 650), P243.
9. Bertog M, Smith DJ, Bielfeld Ackermann A, Bassett J, Ferguson DJ, Korbmacher C & Harris A (2000). Ovine male genital duct epithelial cells differentiate in vitro and express functional CFTR and ENaC. Am J Physiol Cell Physiol 278, C885-C894.
10. Bize V & Horisberger JD (2007). Sodium self-inhibition of human epithelial sodium channel: Selectivity and affinity of the extracellular sodium sensing site. Am J Physiol Renal Physiol 293, F1137-F1146.
11. Canessa CM, Horisberger JD & Rossier BC (1993). Epithelial sodium channel related to proteins involved in neurodegeneration. Nature 361, 467-470.
12. Cuffe JE, Bertog M, Bunnett NW & Korbmacher C (2000). Basolateral proteinase-activated receptor-2 modifies transepithelial ion transport in mouse distal colon. J Physiol 527, 34 P-35 P.
13. + absorption is enhanced in a mouse model for Liddel's syndrome. Pflugers Arch 443 (Suppl.), S282.
14. + absorption in the mouse distal colon. J Physiol 539, 209-222.
15. + channels is maintained in a mouse model of Liddle's syndrome. Am J Physiol Renal Physiol 285, F310-F318.
16. + channel cell surface expression. EMBO J 20, 7052-7059.
17. Diakov A & Korbmacher C (2004). A novel pathway of ENaC activation involves an SGK1 consensus motif in the C-terminus of the channel's α-subunit. J Biol Chem 279, 38134-38142.
18. +. Proc Natl Acad Sci U S A 95, 7169-7173.
19. Epple HJ, Amasheh S, Mankertz J, Goltz M, Schulzke JD & Fromm M (2000). Early aldosterone effect in distal colon by transcriptional regulation of ENaC subunits. Am J Physiol Gastrointest Liver Physiol 278, G718-G724.
20. Escoubet B, Coureau C, Bonvalet JP & Farman N (1997). Noncoordinate regulation of epithelial Na channel and Na pump subunit mRNAs in kidney and colon by aldosterone. Am J Physiol Cell Physiol 272, C1482-C1491.
21. Fakitsas P, Adam G, Daidie D, van Bemmelen MX, Fouladkou F, Patrignani A, Wagner U, Warth R, Camargo SM, Staub O & Verrey F (2007). Early aldosterone-induced gene product regulates the epithelial sodium channel by deubiquitylation. J Am Soc Nephrol 18, 1084-1092.
22. + channel and a mutant causing Liddle syndrome: A quantitative approach. Proc Natl Acad Sci U S A 93, 15370-15375.
23. + absorption in rat late distal colon by nanomolar aldosterone added in vitro. Am J Physiol Endocrinol Metab 264, E68-E73.
24. Fuller PJ, Brennan FE & Burgess JS (2000). Acute differential regulation by corticosteroids of epithelial sodium channel subunit and Nedd4 mRNA levels in the distal colon. Pflugers Arch 441, 94-101.
25. Garty H & Palmer LG (1997). Epithelial sodium channels: Function, structure, and regulation. Physiol Rev 77, 359-396.
26. Greig ER, Baker EH, Mathialahan T, Boot-Handford RP & Sandle GI (2002). Segmental variability of ENaC subunit expression in rat colon during dietary sodium depletion. Pflugers Arch 444, 476-483.
27. + -ATPase in ulcerative colitis. J Pathol 204, 84-92.
28. Gumz ML, Popp MP, Wingo CS & Cain BD (2003). Early transcriptional effects of aldosterone in a mouse inner medullary collecting duct cell line. Am J Physiol Renal Physiol 285, F664-F673.
29. Jasti J, Furukawa H, Gonzales EB & Gouaux E (2007). Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature 449, 316-323.
30. Kellenberger S, Gautschi I, Rossier BC & Schild L (1998). Mutations causing Liddle syndrome reduce sodium-dependent downregulation of the epithelial sodium channel in the Xenopus oocyte expression system. J Clin Invest 101, 2741-2750.
31. Kellenberger S & Schild L (2002). Epithelial sodium channel/ degenerin family of ion channels: A variety of functions for a shared structure. Physiol Rev 82, 735-767.
32. Knight KK, Olson DR, Zhou R & Snyder PM (2006). Liddle's syndrome mutations increase Na + transport through dual effects on epithelial Na + channel surface expression and proteolytic cleavage. Proc Natl Acad Sci U S A 103, 2805-2808.
33. Kunzelmann K & Mall M (2002). Electrolyte transport in the mammalian colon: Mechanisms and implications for disease. Physiol Rev 82, 245-289.
34. Lang F, Bohmer C, Palmada M, Seebohm G, Strutz-Seebohm N & Vallon V (2006). (Patho) physiological significance of the serum- and slucocorticoid-inducible kinase isoforms. Physiol Rev 86, 1151-1178.
35. Letz B, Ackermann A, Canessa CM, Rossier BC & Korbmacher C (1995). Amiloride-sensitive sodium channels in confluent M-1 mouse cortical collecting duct cells. J Membrane Biol 148, 127-141.
36. Liddle GW, Bledsoe T & Coppage WS Jr (1963). A familial renal disorder simulating primary aldosteronism but with negligible aldosterone secretion. Trans Assoc Am Physicians 76, 199-213.
37. + channel and decreases its surface expression in Xenopus oocytes. Mol Biol Cell 9, 3417-3427.
38. + channel by peptidases. Curr Top Dev Biol 78, 23-46.
39. Pradervand S, Vandewalle A, Bens M, Gautschi I, Loffing J, Hummler E, Schild L & Rossier BC (2003). Dysfunction of the epithelial sodium channel expressed in the kidney of a mouse model for Liddle syndrome. J Am Soc Nephrol 14, 2219-2228.
40. Pradervand S, Wang Q, Burnier M, Beermann F, Horisberger JD, Hummler E & Rossier BC (1999). A mouse model for Liddle's syndrome. J Am Soc Nephrol 10, 2527-2533.
41. Randrianarison N, Escoubet B, Ferreira C, Fontayne A, Fowler-Jaeger N, Clerici C, Hummler E, Rossier BC & Planes C (2007). β-Liddle mutation of the epithelial sodium channel increases alveolar fluid clearance and reduces the severity of hydrostatic pulmonary oedema in mice. J Physiol 582, 777-788.
42. + channel in colon, lung and kidney. Pflugers Arch 430, 299-307.
43. Rexhepaj R, Artunc F, Grahammer F, Nasir O, Sandu C, Friedrich B, Kuhl D & Lang F (2006). SGK1 is not required for regulation of colonic ENaC activity. Pflugers Arch 453, 97-105.
44. Robert-Nicoud M, Flahaut M, Elalouf JM, Nicod M, Salinas M, Bens M, Doucet A, Wincker P, Artiguenave F, Horisberger JD, Vandewalle A, Rossier BC & Firsov D (2001). Transcriptome of a mouse kidney cortical collecting duct cell line: Effects of aldosterone and vasopressin. Proc Natl Acad Sci U S A 98, 2712-2716.
45. Ronzaud C, Loffing J, Bleich M, Gretz N, Grone HJ, Schutz G & Berger S (2007). Impairment of sodium balance in mice deficient in renal principal cell mineralocorticoid receptor. J Am Soc Nephrol 18, 1679-1687.
46. Rossier BC, Pradervand S, Schild L & Hummler E (2002). Epithelial sodium channel and the control of sodium balance: Interaction between genetic and environmental factors. Annu Rev Physiol 64, 877-897.
47. Rubera I, Loffing J, Palmer LG, Frindt G, Fowler-Jaeger N, Sauter D, Carroll T, McMahon A, Hummler E & Rossier BC (2003). Collecting duct-specific gene inactivation of αENaC in the mouse kidney does not impair sodium and potassium balance. J Clin Invest 112, 554-565.
48. Saha C, Eckert GJ, Ambrosius WT, Chun TY, Wagner MA, Zhao Q & Pratt JH (2005). Improvement in blood pressure with inhibition of the epithelial sodium channel in blacks with hypertension. Hypertension 46, 481-487.
49. Sandle GI (1998). Salt and water absorption in the human colon: A modern appraisal. Gut 43, 294-299.
50. Schild L, Canessa CM, Shimkets RA, Gautschi I, Lifton RP & Rossier BC (1995). 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 92, 5699-5703.
51. + self-inhibition. Am J Physiol Renal Physiol 290, F1488-F1496.
52. + channel. J Biol Chem 277, 5-8.
53. Soundararajan R, Zhang TT, Wang J, Vandewalle A & Pearce D (2005). A novel role for glucocorticoid-induced leucine zipper protein (GILZ) in ENaC-mediated sodium transport. J Biol Chem 280, 39970-39981.
54. Stockmann M, Gitter AH, Sorgenfrei D, Fromm M & Schulzke JD (1999). Low edge damage container insert that adjusts intestinal forceps biopsies into Ussing chamber systems. Pflugers Arch 438, 107-112.
55. Stokes JB & Sigmund RD (1998). Regulation of rENaC mRNA by dietary NaCl and steroids: Organ, tissue, and steroid heterogeneity. Am J Physiol Cell Physiol 274, C1699-C1707.
56. + transport by aldosterone. In The Kidney, Physiology and Pathophysiology, ed. Seldin DW & Giebisch G, 3rd edn, Chap. 53, pp. 1441-1471. Lippencott Williams and Wilkins, Philadelphia, USA.
57. + -channel (ENaC) by reducing the rate of channel retrieval. Pflugers Arch 447, 884-894.
58. Warnock DG (1998). Liddle syndrome: An autosomal dominant form of human hypertension. Kidney Int 53, 18-24.
59. -channel does not exacerbate the cystic fibrosis phenotype of cystic fibrosis transmembrane conductance regulator mouse models. J Biol Chem 279, 22276-22283.