Rapid stimulation of human renal ENaC by cAMP in Xenopus laevis oocytes
Tóm tắt
Among the compensatory mechanisms restoring circulating blood volume after severe haemorrhage, increased vasopressin secretion enhances water permeability of distal nephron segments and stimulates Na+ reabsorption in cortical collecting tubules via epithelial sodium channels (ENaC). The ability of vasopressin to upregulate ENaC via a cAMP-dependent mechanism in the medium to long term is well established. This study addressed the acute regulatory effect of cAMP on human ENaC (hENaC) and thus the potential role of vasopressin in the initial compensatory responses to haemorrhagic shock. The effects of raising intracellular cAMP (using 5 mmol/L isobutylmethylxanthine (IBMX) and 50 μmol/L forskolin) on wild-type and Liddle-mutated hENaC activity expressed in Xenopus oocytes and hENaC localisation in oocyte membranes were evaluated by dual-electrode voltage clamping and immunohistochemistry, respectively. After 30 min, IBMX + forskolin had stimulated amiloride-sensitive Na+ current by 52 % and increased the membrane density of Na+ channels in oocytes expressing wild-type hENaC. These responses were prevented by 5 μmol/L brefeldin A, which blocks antegrade vesicular transport. By contrast, IBMX + forskolin had no effects in oocytes expressing Liddle-mutated hENaC. cAMP stimulated rapid, exocytotic recruitment of wild-type hENaC into Xenopus oocyte membranes, but had no effect on constitutively over-expressed Liddle-mutated hENaC. Extrapolating these findings to the early cAMP-mediated effect of vasopressin on cortical collecting tubule cells, they suggest that vasopressin rapidly mobilises ENaC to the apical membrane of cortical collecting tubule cells, but does not enhance ENaC activity once inserted into the membrane. We speculate that this stimulatory effect on Na+ reabsorption (and hence water absorption) may contribute to the early restoration of extracellular fluid volume following severe haemorrhage.
Tài liệu tham khảo
Abriel H, Horisberger JD (1999) Feedback inhibition of rat amiloride-sensitive epithelial sodium channels expressed in Xenopus laevis oocytes. J Physiol 516:31–43
Alfaidy N, Blot-Chabaud M, Bonvalet JP, Farman N (1997) Vasopressin potentiates mineralocorticoid selectivity by stimulating 11 beta hydroxysteroid deshydrogenase in rat collecting duct. J Clin Invest 100:2437–2442
Auberson M, Hoffmann-Pochon N, Vandewalle A, Kellenberger S, Schild L (2003) Epithelial Na+ channel mutants causing Liddle’s syndrome retain ability to respond to aldosterone and vasopressin. Am J Physiol Renal Physiol 285:F459–F471
Awayda MS (1999) Regulation of the epithelial Na+ channel by intracellular Na+. Am J Physiol Cell Physiol 277:C216–C224
Awayda MS, Ismailov II, Berdiev BK, Fuller CM, Benos DJ (1996) Protein kinase regulation of a cloned epithelial Na+ channel. J Gen Physiol 108:49–65
Benos DJ, Awayda MS, Ismailov II, Johnson JP (1995) Structure and function of amiloride-sensitive Na+ channels. J Memb Biol 143:1–18
Bubien J, Ismailov I, Berdiev B, Cornwell T, Lifton RP, Fuller CM, Achard JM, Benos DJ, Warnock DG (1996) Liddle’s disease: abnormal regulation of amiloride-sensitive Na+ channels by beta-subunit mutation. Am J Physiol Cell Physiol 270:C208–C213
Butterworth MB, Edinger RS, Johnson JP, Frizzell RA (2005) Acute ENaC stimulation by cAMP in a kidney cell line is mediated by exocytic insertion from a recycling channel pool. J Gen Physiol 125:81–101
Canessa CM, Horisberger JD, Rossier BC (1993) Epithelial sodium channel related to proteins involved in neurodegeneration. Nature 361:467–470
Canessa CM, Schild L, Buell G, Thorens B, Gautschi I, Horisberger JD, Rossier BC (1994) Amiloride-sensitive epithelial Na+ channel is made of three homologous subunits. Nature 367:463–467
Chraibi A, Horisberger J (2003) Dual effect of temperature on the human epithelial Na+ channel. Pflügers Arch 447:316–320
Collier DM, Snyder PM (2011) Identification of ENaC inter-subunit Cl- inhibitory residues suggests a trimeric αγβ channel architecture. J Biol Chem 286:6027–6032
Dijkink L, Hartog A, van Os CH, Bindels RJM (2002) The epithelial sodium channel (ENaC) is intracellularly located as a tetramer. Pflügers Archiv 444:549–555
Ecelbarger CA, Kim GH, Terris J, Masilamani S, Mitchell C, Reyes I, Verbalis JG, Knepper MA (2000) Vasopressin-mediated regulation of epithelial sodium channel abundance in rat kidney. Am J Physiol Renal Physiol 279:F46–F53
Firsov D, Gautschi I, Merillat AM, Rossier BC, Schild L (1998) The heterotetrameric architecture of the epithelial sodium channel (ENaC). EMBO J 17:344–352
Fushimi K, Sasaki S, Marumo F (1997) Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of the aquaporin-2 water channel. J Biol Chem 272:14800–14804
Hansson JH, Nelson-Williams C, Suzuki H, Schild L, Shimkets RA, Lu Y, Canessa CM, Iwasaki T, Rossier BC, Lifton RP (1995) Hypertension caused by a truncated epithelial sodium channel gamma subunit: genetic heterogeneity of Liddle syndrome. Nat Genet 11:76–82
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
Kosari F, Sheng S, Li J, Mak D, Foskett K, Kleyman TR (1998) Subunit stoichiometry of the epithelial sodium channel. J Biol Chem 273:13469–13474
Marunaka Y, Eaton DC (1991) Effect of vasopressin and cAMP on single amiloride-blockable Na channels. Am J Physiol 260:C1071–C1084
Nicco C, Wittner M, DiStefano A, Jounier S, Bankir L, Bouby N (2001) Chronic exposure to vasopressin upregulates ENaC and sodium transport in the rat renal collecting duct and lung. Hypertension 38:1143–1149
Niisato N, Ito Y, Marunaka Y (1999) cAMP stimulates Na+ transport in rat fetal pneumocyte: involvement of a PTK- but not a PKA-dependent pathway. Am J Physiol 277:L727–L736
Reif MC, Troutman SL, Schafer JA (1986) Sodium transport by rat cortical collecting tubule. Effects of vasopressin and desoxycorticosterone. J Clin Invest 77:1291–1298
Schafer JA, Troutman SL (1990) cAMP mediates the increase in apical membrane Na+ conductance produced in rat CCD by vasopressin. Am J Physiol Renal Physiol 259:F823–F831
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 USA 92:5699–5703
Shimkets RA, Lifton RP, Canessa CM (1997) The activity of the epithelial sodium channel is regulated by clathrin-mediated endocytosis. J Biol Chem 272:25537–25541
Shimkets RA, Lifton R, Canessa CM (1998) In vivo phosphorylation of the epithelial sodium channel. Proc Natl Acad Sci USA 95:3301–3305
Shimkets RA, Warnock DG, Bositis CM, Nelson-Williams C, Hansson JH, Schambelan M, Gill JR, Ulick S, Milora RV, Findling JW, Canessa CM, Rossier BC, Lifton RP (1994) Liddle’s syndrome: heritable human hypertension caused by mutations in the β subunit of the epithelial sodium channel. Cell 79:407–414
Snyder PM (2000) Liddle’s syndrome mutations disrupt cAMP-mediated translocation of the epithelial Na+ channel to the cell surface. J Clin Invest 105:45–53
Snyder PM, Olson DR, Kabra R, Zhou R, Steines JC (2004) cAMP and serum and glucocorticoid-inducible kinase (SGK) regulate the epithelial Na+ channel through convergent phosphorylation of Nedd4-2. J Biol Chem 279:45753–45758
Snyder PM, Price MP, McDonald FJ, Adams CM, Volk KA, Zeiher BG, Stokes JB, Welsh MJ (1995) Mechanism by which Liddle’s syndrome mutations increase activity of a human epithelial Na+ channel. Cell 83:969–978
Stewart AP, Haerteis S, Diakov A, Korbmacher C, Edwardson JM (2011) Atomic force microscopy reveals the architecture of the epithelial sodium channel (ENaC). J Biol Chem 286:31944–31952
Stockland JD, Staruschenko A, Pochynyuk O, Booth RE, Silverthorn DU (2008) Insight toward epithelial Na+ channel mechanism revealed by the acid-sensing ion channel 1 structure. IUBMB Life 60:620–628