Colon-specific deletion of epithelial sodium channel causes sodium loss and aldosterone resistance

Journal of the American Society of Nephrology

Volumn 25, Issue 7, 2014, Pages 1453-1464

  Malsure, Sumedha ^a   Wang, Qing ^b,c   Charles, Roch Philippe ^a,d   Sergi, Chloe ^a   Perrier, Romain ^a,f   Christensen, Birgitte Mønster ^a,e   Maillard, Marc ^b   Rossier, Bernard C ^a   Hummler, Edith ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c UNIVERSITY OF FRIBOURG   (Switzerland)

^d UNIVERSITY OF BERN   (Switzerland)

^e AARHUS UNIVERSITY   (Denmark)

^f CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALDOSTERONE; EPITHELIAL SODIUM CHANNEL; PROSTASIN; SERINE PROTEINASE; SODIUM;

ANIMAL; ARTICLE; COLON; FEMALE; MALE; METABOLISM; MOUSE; PHYSIOLOGY;

ALDOSTERONE; ANIMALS; COLON; EPITHELIAL SODIUM CHANNELS; FEMALE; MALE; MICE; SERINE ENDOPEPTIDASES; SODIUM;

EID: 84899539456     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2013090936     Document Type: Article

References (43)

1. Staub O, Loffing J: Mineralocorticoid action in the aldosterone sensitive distal nephron. In: Seldin and Giebisch's The Kidney, 5th Ed., edited by Alpern RJ, MoeOW, CaplanM, London, Academic, 2013, pp 1181-1211
2. Zennaro MC, Jeunemaitre X, Boulkroun S: Integrating genetics and genomics in primary aldosteronism. Hypertension 60: 580-588, 2012
3. Lifton RP: Genetic Diseases of the Kidney, Amsterdam, Elsevier/Academic Press, 2009
4. Canessa CM, Horisberger JD, Rossier BC: Epithelial sodiumchannel related to proteins involved in neurodegeneration. Nature 361: 467-470, 1993
5. Canessa CM, Schild L, Buell G, Thorens B, Gautschi I, Horisberger JD, Rossier BC: Amiloride-sensitive epithelial Na+ channel ismade of three homologous subunits. Nature 367: 463-467, 1994
6. 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-deficientmice. NatGenet 12: 325-328, 1996
7. Barker PM, Nguyen MS, Gatzy JT, Grubb B, Norman H, Hummler E, Rossier B, Boucher RC, Koller B: Role of gammaENaC subunit in lung liquid clearance and electrolyte balance in newborn mice. Insights into perinatal adaptation and pseudohypoaldosteronism. J Clin Invest 102: 1634-1640, 1998
8. McDonald FJ, Yang B, Hrstka RF, Drummond HA, Tarr DE, McCray PB Jr, Stokes JB, Welsh MJ, Williamson RA: Disruption of the beta subunit of the epithelial Na+ channel in mice: Hyperkalemia and neonatal death associated with a pseudohypoaldosteronism phenotype. Proc Natl Acad Sci U S A 96: 1727-1731, 1999
9. Rubera I, Loffing J, Palmer LG, Frindt G, Fowler-Jaeger N, Sauter D, Carroll T, McMahon A, Hummler E, Rossier BC: Collecting duct-specific gene inactivation of alphaENaC in the mouse kidney does not impair sodium and potassium balance. J Clin Invest 112: 554-565, 2003
10. Duc C, Farman N, Canessa CM, Bonvalet JP, Rossier BC: Cell-specific expression of epithelial sodium channel alpha, beta, and gamma subunits in aldosterone-responsive epithelia from the rat: Localization by in situ hybridization and immunocytochemistry. J Cell Biol 127: 1907-1921, 1994
11. Kunzelmann K, Mall M: Electrolyte transport in the mammalian colon: Mechanisms and implications for disease. Physiol Rev 82: 245-289, 2002
12. Koyama K, Sasaki I, Naito H, Funayama Y, Fukushima K, Unno M, Matsuno S, Hayashi H, Suzuki Y: Induction of epithelial Na+ channel in rat ileum after proctocolectomy. Am J Physiol 276: G975-G984, 1999
13. Lingueglia E, Renard S, Waldmann R, Voilley N, Champigny G, Plass H, Lazdunski M, Barbry P: Different homologous subunits of the amiloridesensitive Na+ channel are differently regulated by aldosterone. J Biol Chem 269: 13736-13739, 1994
14. Renard S, Voilley N, Bassilana F, LazdunskiM, Barbry P: Localization and regulation by steroids of the alpha, beta and gamma subunits of the amiloride-sensitive Na+ channel in colon, lung and kidney. Pflügers Arch 430: 299-307, 1995
15. Asher C, Wald H, Rossier BC, Garty H: Aldosterone-induced increase in the abundance of Na+ channel subunits. Am J Physiol 271: C605-C611, 1996
16. Sandle GI: Salt and water absorption in the human colon: A modern appraisal. Gut 43: 294-299, 1998
17. Pradervand S, Wang Q, Burnier M, Beermann F, Horisberger JD, Hummler E, Rossier BC: A mouse model for Liddle's syndrome. J Am Soc Nephrol 10: 2527-2533, 1999
18. Pradervand S, Vandewalle A, BensM, Gautschi I, Loffing J, Hummler E, Schild L, Rossier BC: Dysfunction of the epithelial sodium channel expressed in the kidney of amouse model for Liddle syndrome. J AmSoc Nephrol 14: 2219-2228, 2003
19. 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
20. Amasheh S, Barmeyer C, Koch CS, Tavalali S, Mankertz J, Epple HJ, Gehring MM, Florian P, Kroesen AJ, Zeitz M, Fromm M, Schulzke JD: Cytokine-dependent transcriptional down-regulation of epithelial sodium channel in ulcerative colitis. Gastroenterology 126: 1711-1720, 2004
21. Zeissig S, Bergann T, Fromm A, Bojarski C, Heller F, Guenther U, Zeitz M, Fromm M, Schulzke JD: Altered ENaC expression leads to impaired sodium absorption in the noninflamed intestine in Crohn's disease. Gastroenterology 134: 1436-1447, 2008
22. Vallet V, Chraibi A, Gaeggeler HP, Horisberger JD, Rossier BC: An epithelial serine protease activates the amiloride-sensitive sodium channel. Nature 389: 607-610, 1997
23. Vuagniaux G, Vallet V, Jaeger NF, Hummler E, Rossier BC: Synergistic activation of ENaC by three membrane-bound channel-activating serine proteases (mCAP1, mCAP2, and mCAP3) and serum- and glucocorticoid- regulated kinase (Sgk1) in Xenopus oocytes. J Gen Physiol 120: 191-201, 2002
24. Vuagniaux G, Vallet V, Jaeger NF, Pfister C, Bens M, Farman N, Courtois-CoutryN, Vandewalle A, Rossier BC, Hummler E: Activation of the amiloride-sensitive epithelial sodium channel by the serine protease mCAP1 expressed in a mouse cortical collecting duct cell line. J Am Soc Nephrol 11: 828-834, 2000
25. Adachi M, Kitamura K, Miyoshi T, Narikiyo T, Iwashita K, Shiraishi N, Nonoguchi H, Tomita K: Activation of epithelial sodium channels by prostasin in Xenopus oocytes. J Am Soc Nephrol 12: 1114-1121, 2001
26. Planès C, Randrianarison NH, Charles RP, Frateschi S, Cluzeaud F, Vuagniaux G, Soler P, Clerici C, Rossier BC, Hummler E: ENaC-mediated alveolar fluid clearance and lung fluid balance depend on the channelactivating protease 1. EMBO Mol Med 2: 26-37, 2010
27. Wang Q, Horisberger JD, Maillard M, Brunner HR, Rossier BC, Burnier M: Salt- and angiotensin II-dependent variations in amiloride-sensitive rectal potential difference in mice. Clin Exp Pharmacol Physiol 27: 60-66, 2000
28. Wang H, Garvin JL, Carretero OA: Angiotensin II enhances tubuloglomerular feedback via luminal AT(1) receptors on the macula densa. Kidney Int 60: 1851-1857, 2001
29. Pradervand S, Barker PM, Wang Q, Ernst SA, Beermann F, Grubb BR, BurnierM, Schmidt A, Bindels RJ, Gatzy JT, Rossier BC, Hummler E: Salt restriction induces pseudohypoaldosteronism type 1 in mice expressing low levels of the beta-subunit of the amiloride-sensitive epithelial sodium channel. Proc Natl Acad Sci U S A 96: 1732-1737, 1999
30. Machnik A, Neuhofer W, Jantsch J, Dahlmann A, Tammela T, Machura K, Park JK, Beck FX, Müller DN, Derer W, Goss J, Ziomber A, Dietsch P, WagnerH, van RooijenN, Kurtz A, Hilgers KF, Alitalo K, Eckardt KU, Luft FC, Kerjaschki D, Titze J: Macrophages regulate salt-dependent volume and blood pressure by a vascular endothelial growth factor-Cdependent buffering mechanism. Nat Med 15: 545-552, 2009
31. Sorensen MV, Matos JE, Praetorius HA, Leipziger J: Colonic potassium handling. Pflügers Arch 459: 645-656, 2010
32. Frateschi S, Keppner A, Malsure S, Iwaszkiewicz J, Sergi C, Mérillat AM, Fowler-JaegerN, RandrianarisonN, Planès C, Hummler E:Mutations of the serine protease CAP1/Prss8 lead to reduced embryonic viability, skin defects, and decreased ENaC activity. Am J Pathol 181: 605-615, 2012
33. Hummler E, Dousse A, Rieder A, Stehle JC, Rubera I, Osterheld MC, Beermann F, Frateschi S, Charles RP: The channel-activating protease CAP1/Prss8 is required for placental labyrinth maturation. PLoS One 8: e55796, 2013
34. Leyvraz C, Charles RP, Rubera I, Guitard M, Rotman S, Breiden B, Sandhoff K, Hummler E: The epidermal barrier function is dependent on the serine protease CAP1/Prss8. J Cell Biol 170: 487-496, 2005
35. Frateschi S, Camerer E, Crisante G, Rieser S, Membrez M, Charles RP, Beermann F, Stehle JC, Breiden B, Sandhoff K, Rotman S, Haftek M, Wilson A, Ryser S, SteinhoffM, Coughlin SR, Hummler E: PAR2 absence completely rescues inflammation and ichthyosis caused by altered CAP1/Prss8 expression in mouse skin. Nat Commun 2: 161, 2011
36. Hummler E, MérillatAM, Rubera I, Rossier BC, Beermann F:Conditional gene targeting of the Scnn1a (alphaENaC) gene locus. Genesis 32: 169-172, 2002
37. Rubera I, Meier E, Vuagniaux G, Mérillat AM, Beermann F, Rossier BC, Hummler E: A conditional allele at the mouse channel activating protease 1 (Prss8) gene locus. Genesis 32: 173-176, 2002
38. Sorensen MV, Grossmann S, Roesinger M, Gresko N, Todkar AP, Barmettler G, Ziegler U, Odermatt A, Loffing-Cueni D, Loffing J: Rapid dephosphorylation of the renal sodium chloride cotransporter in response to oral potassium intake in mice. Kidney Int 83: 811-824, 2013
39. Wagner CA, Loffing-Cueni D, Yan Q, Schulz N, Fakitsas P, Carrel M, Wang T, Verrey F, Geibel JP, Giebisch G, Hebert SC, Loffing J: Mouse model of type II Bartter's syndrome. II. Altered expression of renal sodium- and water-transporting proteins. Am J Physiol Renal Physiol 294: F1373-F1380, 2008
40. Planès C, Leyvraz C, Uchida T, AngelovaMA, VuagniauxG, Hummler E, Matthay M, Clerici C, Rossier B: In vitro and in vivo regulation of transepithelial lung alveolar sodiumtransport by serine proteases.AmJ Physiol Lung Cell Mol Physiol 288: L1099-L1109, 2005
41. Meneton P, Schultheis PJ, Greeb J, Nieman ML, Liu LH, Clarke LL, Duffy JJ, Doetschman T, Lorenz JN, Shull GE: Increased sensitivity to K+ deprivation in colonic H, K-ATPase-deficient mice. J Clin Invest 101: 536-542, 1998
42. List K, Kosa P, Szabo R, Bey AL, Wang CB, Molinolo A, Bugge TH: Epithelial integrity is maintained by a matriptase-dependent proteolytic pathway. Am J Pathol 175: 1453-1463, 2009
43. Christensen BM, Perrier R, Wang Q, Zuber AM, Maillard M, Mordasini D, Malsure S, Ronzaud C, Stehle JC, Rossier BC, Hummler E: Sodium and potassium balance depends on aENaC expression in connecting tubule. J Am Soc Nephrol 21: 1942-1951, 2010