Skip to main content

Advertisement

SpringerLink
Log in

Expression and insights on function of potassium channel TWIK-1 in mouse kidney

  • Renal Function, Body Fluids
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

Renal distribution and function of TWIK-1, a member of the two-pore-domain potassium channel family, was studied in mouse kidney. TWIK-1 is expressed in apical and subapical localizations of proximal tubule and cytoplasmic sites of thin and thick ascending limbs, distal convoluted tubules and medullary collecting duct. Studies in mice lacking intact TWIK-1 (twik-1 −/−) and wild-type mice (twik-1 +/+) revealed an attenuated ability to increase renal phosphate (Pi) reabsorption and stabilize plasma Pi concentration in response to a low Pi diet in twik-1 −/− mice. Western blot analysis and immunohistochemistry for the electrogenic 3Na+-1HPO 2−4 -cotransporter NaPi-2a revealed a reduced reno-cortical expression in twik-1 −/− mice under these conditions. Under normal diet, twik-1 −/− mice presented lower urinary flow rates. Acute pharmacologic blockade of the vasopressin V2-receptor revealed both an attenuated diuretic response and an attenuated internalization of aquaporin-2 in the inner medullary collecting duct in twik-1 −/− versus +/+ mice. In summary, mice deficient for TWIK-1 presented impaired regulation of (i) Pi transport in proximal tubule and (ii) water transport in medullary collecting duct. TWIK-1 may contribute to membrane trafficking/expression of transport molecules in proximal tubule and medullary collecting duct, and possibly other renal sites of expression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Arrighi I, Lesage F, Scimeca JC, Carle GF, Barhanin J (1998) Structure, chromosome localization, and tissue distribution of the mouse twik K+ channel gene. FEBS Lett 425:310–316

    Google Scholar 

  2. Cluzeaud F, Reyes R, Escoubet B, Fay M, Lazdunski M, Bonvalet JP, Lesage F, Farman N (1998) Expression of TWIK-1, a novel weakly inward rectifying potassium channel in rat kidney. Am J Physiol 275:C1602–C1609

    Google Scholar 

  3. Decressac S, Franco M, Bendahhou S, Warth R, Knauer S, Barhanin J, Lazdunski M, Lesage F (2004) ARF6-dependent interaction of the TWIK1 K+ channel with EFA6, a GDP/GTP exchange factor for ARF6. EMBO Rep 5(12):1171–1175

    Google Scholar 

  4. Dupe V, Davenne M, Brocard J, Dolle P, Mark M, Dierich A, Chambon P, Rijli FM (1997) In vivo functional analysis of the Hoxa-1 3’ retinoic acid response element (3’ RARE). Development 124:399–410

    Google Scholar 

  5. Huang DY, Pfaff I, Serradeil-Le Gal C, Vallon V (2000) Acute renal response to the non-peptide vasopressin V2-receptor antagonist SR 121463B in anesthetized rats. Naunyn-Schmiedeberg Arch Pharmacol 362:201–207

    Google Scholar 

  6. Huang DY, Wulff P, Volkl H, Loffing J, Richter K, Kuhl D, Lang F, Vallon V (2004) Impaired regulation of renal K+ elimination in the sgk1-knockout mouse. J Am Soc Nephrol 15:885–891

    Google Scholar 

  7. Lesage F (2003) Pharmacology of neuronal background potassium channels. Neuropharmacology 44:1–7

    Google Scholar 

  8. Lesage F, Guillemare E, Fink M, Duprat F, Lazdunski M, Romey G, Barhanin J (1996) TWIK-1, a ubiquitous human weakly inward rectifying K+ channel with a novel structure. EMBO J 15:1004–1011

    Google Scholar 

  9. Lesage F, Lauritzen I, Duprat F, Reyes R, Fink M, Heurteaus C, Lazdunski M (1997) The structure, function and distribution of the mouse TWIK-1 K+ channel. FEBS Lett 402:28–32

    Google Scholar 

  10. Lesage F, Reyes R, Fink M, Duprat F, Guilemare E, Lazdunski M (1996) Dimerization of TWIK-1 K+ channel subunits via a disulfide bridge. EMBO J 15:6400–6407

    Google Scholar 

  11. Loffing J, Loffing-Cueni D, Valderrabano V, Klausli L, Hebert SC, Rossier BC, Hoenderop JG, Bindels RJ, Kaissling B (2001) Distribution of transcellular calcium and sodium transport pathways along mouse distal nephron. Am J Physiol Renal Physiol 281:F1021—F1027

    Google Scholar 

  12. Murer H, Forster I, Biber J (2004) The sodium phosphate cotransporter family SLC34. Pflugers Arch 447:763–767

    Google Scholar 

  13. Nicolas MT, Barhanin J, Reyes R, Dememes D (2003) Cellular localization of TWIK-1, a two-pore-domain potassium channel in the rodent inner ear. Hear Res 181:20–26

    Google Scholar 

  14. Orias M, Velazquez H, Tung F, Lee G, Desir GV (1997) Cloning and localization of a double-pore K channel, KCNK1: exclusive expression in distal nephron segments. Am J Physiol 273:F663–F666

    Google Scholar 

  15. Pfaff IL, Vallon V (2002) Protein kinase C beta isoenzymes in experimental diabetes mellitus and their relation to nephroprotective actions of the ACE inhibitor lisinopril. Kidney Blood Press Res 25:329–340

    Google Scholar 

  16. Pfaff IL, Wagner HJ, Vallon V (1999) Immunolocalization of protein kinase C isoenzymes alpha, beta I and beta II in rat kidney. J Am Soc Nephrol 10:1861–1873

    Google Scholar 

  17. Rajewsky K, Gu H, Kuhn R, Betz UAK, Muller W, Roes J, Schwenk F (1996) Conditional gene targeting. J Clin Invest 98:600–603

    Google Scholar 

  18. Redling S, Pfaff IL, Leitges M, Vallon V (2004) Immunolocalization of protein kinase C isoenzymes alpha, beta I, beta II, delta and epsilon in mouse kidney. Am J Physiol Renal Physiol 287:F289—F298

    Google Scholar 

  19. Riccardi D, Traebert M, Ward DT, Kaissling B, Biber J, Hebert SC, Murer H (2002) Dietary phosphate and parathyroid hormone alter the expression of the calcium-sensing receptor (CaR) and the Na+-dependent Pi transporter (NaPi-2) in the rat proximal tubule. Pflügers Arch 441:379–387

    Google Scholar 

  20. Sands JM, Naruse M, Baum M, Jo I, Hebert SC, Brown EM, Harris HW (1997) Apical extracellular calcium/polyvalent cation-sensing receptor regulates vasopressin-elicited water permeability in rat kidney inner medullary collecting duct. J Clin Invest 15:1399–1405

    Google Scholar 

  21. Talley EM, Solorzano G, Lei Q, Kim D, Bayliss DA (2001) CNS distribution of members of the two-pore-domain (KCNK) potassium channel family. J Neurosci 21:7491–7505

    Google Scholar 

  22. Vallon V, Grahammer F, Richter K, Bleich M, Lang F, Barhanin J, Volkl H, Warth R (2001) Role of KCNE1-dependent K+ fluxes in mouse proximal tubule. J Am Soc Nephrol 12:2003–2011

    Google Scholar 

  23. Wulff P, Vallon V, Huang DY, Volkl H, Yu F, Richter K, Jansen M, Schlünz M, Klingel K, Loffing J, Kauselmann G, Bösl MR, Lang F, Kuhl D (2002) Impaired renal Na+ retention in the sgk1-knockout mouse. J Clin Invest 110:1263–1268

    Google Scholar 

  24. Yao L, Huang DY, Pfaff IL, Nie X, Leitges M, Vallon V (2004) Evidence for a role of protein kinase C alpha in urine concentration. Am J Physiol Renal Physiol 287:F299–F304

    Google Scholar 

Download references

Acknowledgments

The study was supported by Bundesministerium für Bildung, Wissenschaft, Forschung und Technologie (IZKF) 01 KS 9602 and Deutsche Forschungsgemeinschaft (Va 118/7-2) by the Department of Veterans Affairs and the National Institutes of Health (DK56248) and by the Centre National de la Recherche Scientifique (CNRS, France). We thank J. Biber (Institute of Physiology, University of Zuerich) and F. Lesage (CNRS, Sophia Antipolis) for providing anti-NaPi-2a and Twik-1 antisera, respectively. SR121463 was kindly provided by C. Serradeil-Le Gal, Sanofi-Recherche, France.

Author information

Authors and Affiliations

  1. Institute of Pharmacology and Toxicology, University of Tübingen, Germany

    Xin Nie, Imke Pfaff & Volker Vallon

  2. Institut de Pharmacologie Moleculaire et Cellulaire du CNRS, Valbonne, France

    Isabelle Arrighi & Jacques Barhanin

  3. Institute of Anatomy, University of Zürich, Switzerland

    Brigitte Kaissling

  4. Beckmann Research Institute of the City of Hope, Duarte, CA, USA

    Jeffrey Mann

  5. Departments of Medicine and Pharmacology, University of California San Diego and VASDHS, 3350 La Jolla Village Drive (9151), San Diego, CA, 92161, USA

    Volker Vallon

Authors
  1. Xin Nie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Isabelle Arrighi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brigitte Kaissling
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Imke Pfaff
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jeffrey Mann
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jacques Barhanin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Volker Vallon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Volker Vallon.

Additional information

X. Nie and I. Arrighi have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nie, X., Arrighi, I., Kaissling, B. et al. Expression and insights on function of potassium channel TWIK-1 in mouse kidney. Pflugers Arch - Eur J Physiol 451, 479–488 (2005). https://doi.org/10.1007/s00424-005-1480-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-005-1480-9

Keywords

Search

Navigation