Abstract
Volume-sensitive chloride and potassium currents were studied, using the whole-cell clamp technique, in cultured wild-type mouse proximal convoluted tubule (PCT) epithelial cells and compared with those measured in PCT cells from null mutant kcne1 −/− mice. In wild-type PCT cells in primary culture, a Cl− conductance activated by cell swelling was identified. The initial current exhibited an outwardly rectifying current-voltage (I-V) relationship, whereas steady-state current showed decay at depolarized membrane potentials. The ion selectivity was I− > Br− > Cl− >> gluconate. This conductance was sensitive to 1 mM 4,4′-Diisothiocyanostilbene-2,2′-disulfonic acid (DIDS), 0.1 mM 5-nitro-2-(3-phenylpropylamino)benzoic acid (NPPB) and 1 mM diphenylamine-2-carboxylate (DPC). Osmotic stress also activated K+ currents. These currents are time-independent, activated at depolarized potentials, and inhibited by 0.5 mM quinidine, 5 mM barium, and 10 µM clofilium but are insensitive to 1 mM tetraethylammonium (TEA), 10 nM charybdotoxin (CTX), and 10 µM 293B. In contrast, the null mutation of kcne1 completely impaired volume-sensitive chloride and potassium currents in PCT. The transitory transfection of kcne1 restores both Cl− and K+ swelling-activated currents, confirming the implication of KCNE1 protein in the cell-volume regulation in PCT cells in primary cultures.
Similar content being viewed by others
References
A. Arrazola R. Rota P. Hannaert A. Soler R.P. Garay (1993) ArticleTitleCell volume regulation in rat thymocytes. J. Physiol. 465 403–414 Occurrence Handle1:STN:280:ByuD2cnmsVM%3D Occurrence Handle8229842
B. Attali E. Guillemare F. Lesage E. Honore G. Romey M. Lazdunski J. Barhanin (1993) ArticleTitleThe protein IsK is a dual activator of K+ and Cl− channels. Nature 365 850–852 Occurrence Handle1:CAS:528:DyaK2cXlsVCq Occurrence Handle8413671
J. Barhanin F. Lesage E. Guillemare M. Fink M. Lazdunski G. Romey (1996) ArticleTitleK(V)LQT1 and IsK (minK) proteins associate to form the I(Ks) cardiac potassium current. Nature 384 78–80 Occurrence Handle1:CAS:528:DyaK28XmvVegs7c%3D Occurrence Handle8900282
I. Ben-Efraim Y. Shai B. Attali (1996) ArticleTitleCytoplasmic and extracellular IsK peptides activate endogenous K+ and Cl− channels in Xenopus oocytes. Evidence for regulatory function. J. Biol. Chem. 271 8768–8771 Occurrence Handle10.1074/jbc.271.15.8768 Occurrence Handle8621512
M. Bidet M. Tauc I. Rubera G. de Renzis C. Poujeol M.T. Bohn P. Poujeol (1996) ArticleTitleCalcium-activated chloride currents in primary cultures of rabbit distal convoluted tubule. Am. J. Physiol. 271 F940–F950 Occurrence Handle8898026
M. Bleich R. Warth (2000) ArticleTitleThe very small-conductance K+ channel KvLQT1 and epithelial function. Pfluegers Arch. 440 202–206
A. Boucherot R. Schreiber K. Kunzehmann (2001) ArticleTitleRegulation and properties of KCNQ1 (K(V)LQT1) and impact of the cystic fibrosis transmembrane conductance regulator. J. Membrane Biol. 182 39–47
A.E. Busch M. Varnum J.P. Adelman R.A. North (1992) ArticleTitleHypotonic solution increases the slowly activating potassium current IsK expressed in Xenopus oocytes. Biochem. Biophys. Res. Commun. 184 804–810 Occurrence Handle1374241
C. Chouabe N. Neyroud P. Guicheney M. Lazdunski G. Romey J. Barhanin (1997) ArticleTitleProperties of KvLQT1 K+ channel mutations in Romano-Ward and Jervell and Lange-Nielsen inherited cardiac arrhythmias. Embo J. 16 5472–5479 Occurrence Handle10.1093/emboj/16.17.5472 Occurrence Handle9312006
S. Demolombe D. Franco P. de Boer S. Kuperschmidt D. Roden Y. Pereon A. Jarry A.F. Moorman D. Escande (2001) ArticleTitleDifferential expression of KvLQT1 and its regulator IsK in mouse epithelia. Am. J. Physiol. 280 C359–C372
J.L. Eveloff D.G. Warnock (1987) ArticleTitleActivation of ion transport systems during cell volume regulation. Am. J. Physiol. 252 F1–F10 Occurrence Handle3544865
L.C. Freeman R.S. Kass (1993) ArticleTitleExpression of a minimal K+ channel protein in mammalian cells and immunolocalization in guinea pig heart. Circ. Res. 73 968–973 Occurrence Handle1:CAS:528:DyaK2cXls12k Occurrence Handle8403266
R. Frizzell A. Morris (1994) ArticleTitleChloride conductance of salt-secreting epithelial cells. Curr. Top. Membr.: Chloride Channels 173–214
I.A. Greenwood L.J. Miller S. Ohya B. Horowitz (2002) ArticleTitleThe large conductance potassium channel beta-subunit can interact with and modulate the functional properties of a calcium-activated chloride channel, CLCA1. J. Biol. Chem. 277 22119–22222 Occurrence Handle10.1074/jbc.C200215200 Occurrence Handle1:CAS:528:DC%2BD38XltVGksrY%3D Occurrence Handle11994272
R. Greger E. Schlatter (1984) ArticleTitleMechanism of NaCl secretion in the rectal gland of spiny dogfish (Squalus acanthias). I. Experiments in isolated in vitro perfused rectal gland tubules. Pfluegers Arch. 402 63–75
E.K. Hoffmann (2000) ArticleTitleIntracellular signalling involved in volume regulatory decrease. Cell Physiol. Biochem. 10 273–288 Occurrence Handle10.1159/000016356 Occurrence Handle1:CAS:528:DC%2BD3MXjt1alu7k%3D Occurrence Handle11125206
E.K. Hoffmann C. Hougaard (2001) ArticleTitleIntracellular signalling involved in activation of the volume-sensitive K+ current in Ehrlich ascites tumour cells. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 130 355–366 Occurrence Handle10.1016/S1095-6433(01)00419-6 Occurrence Handle1:STN:280:DC%2BD387nvFOktw%3D%3D Occurrence Handle11913449
M.E. Jurman L.M. Boland Y Liu G. Yellen (1994) ArticleTitleVisual identification of individual transfected cells for electrophysiology using antibody-coated beads. Biotechniques 17 876–881 Occurrence Handle1:CAS:528:DyaK2cXmvFKntbo%3D Occurrence Handle7840967
C. Knoblauch M.H. Montrose H. Murer (1989) ArticleTitleRegulatory volume decrease by cultured renal cells. Am. J. Physiol. 256 C252–C259 Occurrence Handle1:STN:280:BiaC2cfktFE%3D Occurrence Handle2919656
S. le Maout M. Tauc N. Koechlin P. Poujeol (1990) ArticleTitlePolarized 86Rb+ effluxes in primary cultures of rabbit kidney proximal cells: role of calcium ana hypotonicity. Biochim. Biophys. Acta 1026 29–39 Occurrence Handle10.1016/0005-2736(90)90328-L Occurrence Handle1:CAS:528:DyaK3cXkvFGhsrg%3D Occurrence Handle2165808
H. Lock M.A. Valverde (2000) ArticleTitleContribution of the IsK (MinK) potassium channel subunit to regulatory volume decrease in murine tracheal epithelial cells. J. Biol. Chem. 275 34849–34852 Occurrence Handle10.1074/jbc.C000633200 Occurrence Handle1:CAS:528:DC%2BD3cXotFeisrc%3D Occurrence Handle10995738
R.J. MacLeod J.R. Hamilton (1996) ArticleTitleActivation of Na+/H+ exchange is required for regulatory volume decrease after modest “physiological” volume increases in jejunal villus epithelial cells. J. Biol. Chem. 271 23138–23145 Occurrence Handle10.1074/jbc.271.18.10654 Occurrence Handle1:CAS:528:DyaK28XlvVChu7w%3D Occurrence Handle8798507
M. Mall A. Wissner R. Schreiber J. Kuehr H.H. Seydewitz M. Brandis R. Greger K. Kunzelmann (2000) ArticleTitleRole of K(V)LQT1 in cyclic adenosine monophosphate-mediated Cl− secretion in human airway epithelia. Am. J. Respir. Cell Mol. Biol. 23 283–289 Occurrence Handle1:CAS:528:DC%2BD3cXntVSht70%3D Occurrence Handle10970817
J. Merot M. Bidet B. Gachot S. Le Maout N. Koechlin M. Tauc P. Poujeol (1989) ArticleTitleElectrical properties of rabbit early distal convoluted tubule in primary culture. Am. J. Physiol. 257 F288–F299 Occurrence Handle1:STN:280:BiaA2cbktlI%3D Occurrence Handle2569836
J. Merot V. Poncet M. Bidet M. Tauc P. Poujeol (1991) ArticleTitleApical membrane ionic channels in the rabbit cortical thick ascending limb in primary culture. Biochim. Biophys. Acta 1070 387–400 Occurrence Handle10.1016/0005-2736(91)90079-N Occurrence Handle1:CAS:528:DyaK38Xls1alsg%3D%3D Occurrence Handle1684913
J.R. Moorman C.J. Palmer J.E. John 3rd M.E. Durieux L.R. Jones (1992) ArticleTitlePhospholemman expression induces a hyperpolarization-activated chloride current in Xenopus oocytes. J. Biol. Chem. 267 14551–14554 Occurrence Handle1:CAS:528:DyaK38XltVyqt7w%3D Occurrence Handle1378834
M.I. Niemeyer L.P. Cid L.F. Barros F.V. Sepulveda (2001) ArticleTitleModulation of the two-pore domain acid-sensitive K+ channel TASK-2 (KCNK5) by changes in cell volume. J. Biol. Chem. 276 43166–43174 Occurrence Handle10.1074/jbc.M107192200 Occurrence Handle1:CAS:528:DC%2BD3MXptleltrY%3D Occurrence Handle11560934
V. Poncet M. Tauc M. Bidet P. Poujeol (1994) ArticleTitleChloride channels in apical membrane of primary cultures of rabbit distal bright convoluted tubule. Am. J. Physiol. 266 F543–F553 Occurrence Handle1:CAS:528:DyaK2cXjtF2qsL0%3D Occurrence Handle8184886
I. Rubera M. Tauc M. Bidet C. Poujeol B. Cuiller A. Watrin N. Touret P. Poujeol (1998) ArticleTitleChloride currents in primary cultures of rabbit proximal and distal convoluted tubules. Am. J. Physiol. 275 F651–F663 Occurrence Handle9815124
I. Rubera M. Tauc F. Michel C. Poujeol P. Poujeol (1997a) ArticleTitleSimultaneous functional expression of swelling and forskolin-activated chloride currents in primary cultures of rabbit distal convoluted tubule. C. R. Acad. Sci. III 320 223–232 Occurrence Handle1:CAS:528:DyaK2sXnt1aitr8%3D
I. Rubera M. Tauc. C. Poujeol M.T. Bohn M. Bidet G. De Renzis P. Poujeol (1997b) ArticleTitleCl− and K+ conductances activated by cell swelling in primary cultures of rabbit distal bright convoluted tubules. Am. J. Physiol. 273 F680–F697 Occurrence Handle1:CAS:528:DyaK2sXnsVCrsLc%3D
N. Shiga P. Wangemann (1995) ArticleTitleIon selectivity of volume regulatory mechanisms present during a hypoosmotic challenge in vestibular dark cells. Biochim. Biophys. Acta 1240 48–54 Occurrence Handle10.1016/0005-2736(95)00175-1 Occurrence Handle1:CAS:528:DyaK2MXpslGrtLg%3D Occurrence Handle7495847
K. Strange (1988) ArticleTitleRVD in principal and intercalated cells of rabbit cortical collecting tubule. Am. J. Physiol. 255 C612–C621 Occurrence Handle1:STN:280:BiaD2cjnsFM%3D Occurrence Handle3189530
T. Sugimoto Y. Tanabe R. Shigemoto M. Iwai T. Takumi H. Ohkubo S. Nakanishi (1990) ArticleTitleImmunohistochemical study of a rat membrane protein which induces a selective potassium permeation: its localization in the apical membrane portion of epithelial cells. J. Membrane Biol. 113 39–47 Occurrence Handle1:CAS:528:DyaK3cXhtFKhsrs%3D
T. Takumi H. Ohkubo S. Nakanishi (1988) ArticleTitleCloning of a membrane protein that induces a slow voltage-gated potassium current. Science 242 1042–1045 Occurrence Handle1:CAS:528:DyaL1MXksFWlsLw%3D Occurrence Handle3194754
M. Tauc M. Bidet P. Poujeol (1996) ArticleTitleChloride currents activated by calcitonin and cAMP in primary cultures of rabbit distal convoluted tubule. J. Membrane Biol. 150 255–273 Occurrence Handle10.1007/s002329900049 Occurrence Handle1:CAS:528:DyaK28XisFGksbk%3D
M. Tauc S. Le Maout P. Poujeol (1990) ArticleTitleFluorescent video-microscopy study of regulatory volume decrease in primary culture of rabbit proximal convoluted tubule. Biochim. Biophys. Acta 1052 278–284 Occurrence Handle10.1016/0167-4889(90)90222-Y Occurrence Handle1:CAS:528:DyaK3cXksFKnt7g%3D Occurrence Handle2334737
V. Vallon F. Grahammer K. Richter M. Bleich F. Lang J. Barhanin H. Volkl R. Warth (2001) ArticleTitleRole of KCNE1-dependent K+ fluxes in mouse proximal tubule. J. Am. Soc. Nephrol. 12 2003–2011 Occurrence Handle1:CAS:528:DC%2BD3MXnsFWitbs%3D Occurrence Handle11562398
C.G. Vanoye L. Reuss (1999) ArticleTitleStretch-activated single K+ channels account for whole-cell currents elicited by swelling. Proc. Natl. Acad. Sci. USA 96 6511–6516 Occurrence Handle10.1073/pnas.96.11.6511 Occurrence Handle1:CAS:528:DyaK1MXksFKktbg%3D Occurrence Handle10339619
D.E. Vetter J.R. Mann P. Wangemann J. Liu K.J. McLaughlin F. Lesage D.C. Marcus M. Lazdunski S.F. Heinemann J. Barhanin (1996) ArticleTitleInner ear defects induced by null mutation of the isk gene. Neuron 17 1251–1264 Occurrence Handle1:CAS:528:DyaK2sXislGntA%3D%3D Occurrence Handle8982171
S. vom Dahl F. Schliess D. Graf D. Haussinger (2001) ArticleTitleRole of p38(MAPK) in cell volume regulation of perfused rat liver. Cell Physiol. Biochem. 11 285–294 Occurrence Handle10.1159/000047815 Occurrence Handle1:CAS:528:DC%2BD38XotF2ktA%3D%3D Occurrence Handle11832654
P. Wangemann J. Liu Z. Shen A. Shipley D.C. Marcus (1995) ArticleTitleHypo-osmotic challenge stimulates transepithelial K+ secretion and activates apical IsK channel in vestibular dark cells. J. Membrane Biol. 147 263–273 Occurrence Handle1:CAS:528:DyaK2MXovFOlurY%3D
R. Warth N. Riedemann M. Bleich W. Van Driessche A.E. Busch R. Greger (1996) ArticleTitleThe cAMP-regulated and 293B-inhibited K+ conductance of rat colonic crypt base cells. Pfluegers Arch. 432 81–88 Occurrence Handle10.1007/s004240050108 Occurrence Handle1:STN:280:BymB2s%2FhtlY%3D
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Barrière, H., Rubera, I., Belfodil, R. et al. Swelling-activated Chloride and Potassium Conductance in Primary Cultures of Mouse Proximal Tubules. Implication of KCNE1 Protein . J. Membrane Biol. 193, 153–170 (2003). https://doi.org/10.1007/s00232-003-2014-z
Received:
Issue Date:
DOI: https://doi.org/10.1007/s00232-003-2014-z