Pflügers Archiv - European Journal of Physiology

, Volume 462, Issue 6, pp 871–883 | Cite as

The inositol Inpp5k 5-phosphatase affects osmoregulation through the vasopressin-aquaporin 2 pathway in the collecting system

  • Eileen Pernot
  • Sara Terryn
  • Siew Chiat Cheong
  • Nicolas Markadieu
  • Sylvie Janas
  • Marianne Blockmans
  • Monique Jacoby
  • Valérie Pouillon
  • Stéphanie Gayral
  • Bernard C. Rossier
  • Renaud Beauwens
  • Christophe Erneux
  • Olivier Devuyst
  • Stéphane Schurmans
Molecular and Genomic Physiology

Abstract

Inositol Inpp5k (or Pps, SKIP) is a member of the inositol polyphosphate 5-phosphatases family with a poorly characterized function in vivo. In this study, we explored the function of this inositol 5-phosphatase in mice and cells overexpressing the 42-kDa mouse Inpp5k protein. Inpp5k transgenic mice present defects in water metabolism characterized by a reduced plasma osmolality at baseline, a delayed urinary water excretion following a water load, and an increased acute response to vasopressin. These defects are associated with the expression of the Inpp5k transgene in renal collecting ducts and with alterations in the arginine vasopressin/aquaporin-2 signalling pathway in this tubular segment. Analysis in a mouse collecting duct mCCD cell line revealed that Inpp5k overexpression leads to increased expression of the arginine vasopressin receptor type 2 and increased cAMP response to arginine vasopressin, providing a basis for increased aquaporin-2 expression and plasma membrane localization with increased osmotically induced water transport. Altogether, our results indicate that Inpp5k 5-phosphatase is important for the control of the arginine vasopressin/aquaporin-2 signalling pathway and water transport in kidney collecting ducts.

Keywords

Water transport Aquaporin Phosphoinositide metabolism 5-Phosphatase Collecting duct 

Notes

Acknowledgements

We thank Y. Maréchal (IRIBHM, IBMM), A. Ahrabi and H. Belge (Division of Nephrology, UCL) for discussions, C. Moreau (IRIBHM), H. Debaix, V. Beaujean and Y. Cnops (Division of Nephrology, UCL) for technical assistance, and D. Trono (Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland) for lentiviral reagents. This work was supported by the Fonds de la Recherche Scientifique-FNRS (FRS-FNRS)(to V.P., S.S., C.E. and O.D.), the Fonds pour la Formation à la Recherche dans l’Industrie et dans l’Agriculture (FRIA)(fellowships to E.P., M.B. and M.J.), the Fonds de la Recherche Scientifique Médicale (FRSM) (to S.S., C.E. and O.D.), the Fonds David et Alice Van Buuren (to M.J.), the Fondation Rose et Jean Hoguet (to E.P.), and a Concerted Research Action (05/10-328), The Chaire Spadel “Eau et Santé” at the UCL (O.D.), an Inter-University Attraction Pole (IUAP P6/05 to O.D.; IUAP P6/28 to C.E.), the NCCR Kidney CH program of the Swiss National Science Foundation and the EUNEFRON project of the European Community (FP7) to O.D.

Supplementary material

424_2011_1028_MOESM1_ESM.doc (35 kb)
Supplementary Table 1Primers sequences (DOC 35 kb)
424_2011_1028_MOESM2_ESM.doc (28 kb)
Supplementary Table 2Baseline parameters, renal function and water metabolism in Inpp5k transgenic mice (DOC 28 kb)
424_2011_1028_MOESM3_ESM.doc (28 kb)
Supplementary Information(DOC 28 kb)
424_2011_1028_MOESM4_ESM.doc (24 kb)
Supplementary Figure Legends(DOC 24.5 kb)
424_2011_1028_MOESM5_ESM.pdf (158 kb)
Supplementary Figure 1(PDF 158 kb)
424_2011_1028_MOESM6_ESM.pdf (79 kb)
Supplementary Figure 2(PDF 78.9 kb)
424_2011_1028_MOESM7_ESM.pdf (136 kb)
Supplementary Figure 3(PDF 136 kb)
424_2011_1028_MOESM8_ESM.pdf (58 kb)
Supplementary Figure 4(PDF 57.6 kb)

References

  1. 1.
    Arhabi AH, Terryn S, Valenti G, Caron N, Serradeil-Le Gal C, Raufaste D, Nielsen S, Horie S, Verbavatz JM, Devuyst O (2007) PKD1 haploinsufficiency causes a syndrome of inappropriate antidiuresis in mice. J Am Soc Nephrol 18:1740–1753CrossRefGoogle Scholar
  2. 2.
    Astle MV, Seaton G, Davies EM, Fedele CG, Rahman P, Arsala L, Mitchell CA (2006) Regulation of phosphoinosotide signaling by the inositol polyphosphate 5-phosphatases. IUBMB Life 58:451–456PubMedCrossRefGoogle Scholar
  3. 3.
    Astle MV, Horan KA, Ooms LM, Mitchell CA (2007) The inositol polyphosphate 5-phosphatases: traffic controllers, waistline watchers and tumor suppressors? Biochem Soc Symp 12:2836–2848Google Scholar
  4. 4.
    Barlow CA, Laishram RS, Anderson RA (2010) Nuclear phosphoinositides: a signaling enigma wrapped in a compartmental conundrum. Trends Cell Biol 20:25–35PubMedCrossRefGoogle Scholar
  5. 5.
    Belge H, Gailly P, Schwaller B, Loffing J, Debaix H, Riveira-Munoz E, Beauwens R, Devogelaer JP, Hoendero JG, Bindels RJ, Devuyst O (2007) Renal expression of parvalbumin is critical for NaCl handling and response to diuretics. Proc Natl Acad Sci USA 104:14849–14854PubMedCrossRefGoogle Scholar
  6. 6.
    Bielas SL, Silhavy JL, Brancati F, Kisseleva MV, Al-Gazali L, Sztriha L, Bayoumi RA, Zaki MS, Abdel-Aleem A, Rosti O, Kayserili H, Swistun D, Scott LC, Bertini E, Boltshauser E, Fazzi E, Travaglini L, Field SJ, Gayral S, Jacoby M, Schurmans S, Dallapiccola B, Majerus PW, Valente EM, Gleeson JG (2009) Mutations in the inositol polyphosphate-5-phosphatase E gene link phosphatidylinositol signaling to the ciliopathies. Nature Genetics 41:1032–1036PubMedCrossRefGoogle Scholar
  7. 7.
    Blero D, Payrastre B, Schurmans S, Erneux C (2007) Phosphoinositide phosphatases in a network of signaling reactions. Pflug Arch Eur J Phys 455:31–44CrossRefGoogle Scholar
  8. 8.
    Christensen BM, Zelenina M, Aperia A, Nielsen S (2000) Localization and regulation of PKA-phosphorylated AQP2 in response to V2-receptor agonist/antagonist treatment. Am J Physiol Renal Physiol 278:F29–F42PubMedGoogle Scholar
  9. 9.
    Christensen EI, Devuyst O, Dom G, Nielsen R, Van der Smissen P, Verroust P, Leruth M, Guggino WB, Courtoy PJ (2003) Loss of chloride channel ClC-5 impairs endocytosis by defective trafficking of megalin and cubilin in kidney proximal tubules. Proc Natl Acad Sci USA 100:8472–8477PubMedCrossRefGoogle Scholar
  10. 10.
    Clément S, Krause U, Desmedt F, Tanti JF, Behrends J, Pesesse X, Sasaki T, Penninger J, Doherty M, Malaisse W, Dumont JE, Le Marchand-Brustel Y, Erneux C, Hue L, Schurmans S (2001) The lipid phosphatase SHIP2 controls insulin sensitivity. Nature 409:92–96PubMedCrossRefGoogle Scholar
  11. 11.
    Communi D, Lecocq R, Erneux C (1996) Arginine 343 and 350 are two active residues involved in substrate binding by human type 1 d-myo-inositol 1,4,5-trisphosphate 5-phosphatase. J Biol Chem 271:11676–11683PubMedCrossRefGoogle Scholar
  12. 12.
    Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–657PubMedCrossRefGoogle Scholar
  13. 13.
    Downes CP, Gray A, Lucocq JM (2005) Probing phosphoinositide functions in signalling and membrane trafficking. Trends Cell Biol 15:259–268PubMedCrossRefGoogle Scholar
  14. 14.
    Gaeggeler HP, Gonzalez-Rodriguez E, Jaeger NF, Loffing-Cueni D, Norregaard R, Loffing J, Horisberger JD, Rossier BC (2005) Mineralocorticoid versus glucocorticoid receptor occupancy mediating aldosteronestimulated sodium transport in a novel renal cell line. J Am Soc Nephrol 16:878–889PubMedCrossRefGoogle Scholar
  15. 15.
    Gaeggeler HP, Guillod Y, Loffing-Cueni D, Loffing J, Rossier BC (2010) Vasopressin-dependent coupling between sodium transport and water flow in a mouse cortical collecting duct cell line. Kidney Int, Dec 22, Epub ahead of print.Google Scholar
  16. 16.
    Gurung R, Tan A, Ooms LM, McGrath MJ, Huysmans RD, Munday AD, Prescott M, Whisstock JC, Mitchell CA (2003) Identification of a novel domain in two mammalian inositol-polyphosphate 5-phosphatases that mediates membrane ruffle localization. J Biol Chem 278:11376–11385PubMedCrossRefGoogle Scholar
  17. 17.
    Halstead JR, Jalink K, Divecha N (2005) An emerging role for PtdIns(4,5)P2-mediated signalling in human disease. Trends Pharmacol Sci 26:654–660PubMedCrossRefGoogle Scholar
  18. 18.
    Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, Meyer T (2006) PI(3,4,5)P3 and PI(4,5)P2 lipid target proteins with polybasic clusters to the plasma membrane. Science 314:1458–1461PubMedCrossRefGoogle Scholar
  19. 19.
    Ijuin T, Mochizuki Y, Fukami K, Funaki M, Asano T, Takenawa T (2000) Identification and characterization of a novel inositol polyphosphate 5-phosphatase. J Biol Chem 275:10870–10875PubMedCrossRefGoogle Scholar
  20. 20.
    Ijuin T, Takenawa T (2003) SKIP negatively regulates insulin-induced GLUT4 translocation and membrane ruffle formation. Mol Cell Biol 23:1209–1220PubMedCrossRefGoogle Scholar
  21. 21.
    Ijuin T, Yu YE, Mizutani K, Pao A, Tateya S, Tamori Y, Bradley A, Takenawa T (2008) Increased insulin action in SKIP heterozygous knockout mice. Mol Cell Biol 28:5184–5195PubMedCrossRefGoogle Scholar
  22. 22.
    Jacoby M, Cox JJ, Gayral S, Hampshire DJ, Ayub M, Blockmans M, Pernot E, Kisseleva MV, Compère P, Schiffmann SN, Gergely F, Riley JH, Pérez-Morga D, Woods GC, Schurmans S (2009) INPP5E mutations cause primary cilium signaling defects, ciliary instability and ciliopathies in human and mouse. Nat Genet 41:1027–1031PubMedCrossRefGoogle Scholar
  23. 23.
    Jänne PA, Suchy SF, Bernard D, McDonald M, Crawley J, Grinberg A, Wynshaw-Boris A, Westphal H, Nussbaum RL (1998) Functional overlap between murine Inpp 5b and Ocrl1 may explain why deficiency of the murine ortholog for OCRL1 does not cause Lowe syndrome in mice. J Clin Invest 101:2042–2053PubMedCrossRefGoogle Scholar
  24. 24.
    Jouret F, Bernard A, Hermans C, Dom G, Terryn S, Leal T, Lebecque P, Cassiman JJ, Scholte BJ, de Jonge HR, Courtoy PJ, Devuyst O (2007) Cystic fibrosis is associated with a defect in apical receptor-mediated endocytosis in mouse and human kidney. J Am Soc Nephrol 18:707–718PubMedCrossRefGoogle Scholar
  25. 25.
    Kagawa S, Soeda Y, Ishihara H, Oya T, Sasahara M, Yaguchi S, Oshita R, Wada T, Tsuneki H, Sasaoka T (2008) Impact of transgenic overexpression of SH2-containing inositol 5′-phosphatase 2 on glucose metabolism and insulin signalling in mice. Endocrinology 149:642–650PubMedCrossRefGoogle Scholar
  26. 26.
    Kaisaki PJ, Delépine M, Woon PY, Sebag-Montefiore L, Wilder SP, Menzel S, Vionnet N, Marion E, Riveline JP, Charpentier G, Schurmans S, Levy JC, Lathrop M, Farrall M, Gauguier D (2004) Polymorphisms in type-II SH2 domain-containing inositol 5-phosphatase (INPPL1, SHIP2) are associated with physiological abnormalities of the metabolic syndrome. Diabetes 53:1900–1904PubMedCrossRefGoogle Scholar
  27. 27.
    Keune WJ, Boultsma Y, Sommer L, Jones D, Divecha N (2010) Phosphoinositide signaling in the nucleus. Adv Enzyme Regul, Oct. 28, Epub ahead of print.Google Scholar
  28. 28.
    Lemmon MA (2008) Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 9:99–111PubMedCrossRefGoogle Scholar
  29. 29.
    Ling K, Schill NJ, Wagoner MP, Sun Y, Anderson RA (2006) Movin’ on up: the role of PtdIns(4,5)P2 in cell migration. Trends Cell Biol 16:276–284PubMedCrossRefGoogle Scholar
  30. 30.
    Liu Y, Bankaitis VA (2010) Phosphoinositide phosphatases in cell biology and diseases. Prog Lipid Res 49:201–217PubMedCrossRefGoogle Scholar
  31. 31.
    Marion E, Kaisaki P, Pouillon V, Gueydan C, Levy JC, Bodson A, Krzentowski G, Daubresse JC, Mockel J, Behrends J, Servais G, Szpirer C, Kruys V, Gauguier D, Schurmans S (2002) The gene INPPL1, encoding the lipid phosphatase SHIP2, is a candidate for type 2 diabetes in rat and man. Diabetes 51:2012–2017PubMedCrossRefGoogle Scholar
  32. 32.
    McCrea HJ, De Camilli P (2009) Mutations in phosphoinositide metabolizing enzymes and human disease. Physiology (Bethesda) 24:8–16CrossRefGoogle Scholar
  33. 33.
    Ooms LM, Horan KA, Rahman P, Seaton G, Gurung R, Kathesparan DS, Mitchell CA (2009) The role of the inositol polyphosphate 5-phosphatases in cellular function and human disease. Biochem J 419:29–49PubMedCrossRefGoogle Scholar
  34. 34.
    Sleeman MW, Wortley KE, Lai KMV, Gowen LC, Kintner J, Kline WO, Garcia K, Stitt TN, Yancopoulos GD, Wiegand SJ, Glass DJ (2005) Absence of the lipid phosphatise SHIP2 confers resistance to dietary obesity. Nat Med 11:199–205PubMedCrossRefGoogle Scholar
  35. 35.
    Suh BC, Hille B (2005) Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate. Curr Opin Neurobiol 15:370–378PubMedCrossRefGoogle Scholar
  36. 36.
    Trebak M, Lemonnier L, Dehaven WI, Wedel BJ, Bird GS, Putney JW Jr (2009) Complex functions of phosphatidylinositol 4,5-bisphosphate in regulation of TRPC5 cation channels. Pflugers Arch 457:757–769PubMedCrossRefGoogle Scholar
  37. 37.
    Vandeput F, Backers K, Villeret V, Pesesse X, Erneux C (2006) The influence of anionic lipids on SHIP2 phosphatidylinositol 3,4,5-trisphosphate 5-phosphatase activity. Cell Signal 18:2193–2199PubMedCrossRefGoogle Scholar
  38. 38.
    Wada T, Sasaoka T, Funaki M, Hori H, Murakami S, Ishiki M, Haruta Y, Asano T, Ogawa W, Ishihara H, Kobayashi M (2001) Overexpression of SH2-containing inositol phosphatise 2 results in negative regulation of insulin-induced metabolic actions in 3T3-L1 adipocytes via its 5′-phosphatase catalytic activity. Mol Cell Biol 21:1633–1646PubMedCrossRefGoogle Scholar
  39. 39.
    Xiong Q, Deng CY, Chai J, Jiang SW, Xiong YZ, Li FE, Zheng R (2009) Knockdown of endogenous SKIP gene enhanced insulin-induced glycogen synthesis signalling in differentiating C2C12 myoblasts. BMB Rep 42:119–124PubMedCrossRefGoogle Scholar
  40. 40.
    Yu H, Fukami K, Watanabe Y, Ozaki C, Takenawa T (1998) Phosphatidylinositol 4,5-bisphosphate reverses the inhibition of RNA transcription caused by histone H1. Eur J Biochem 251:281–287PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Eileen Pernot
    • 1
    • 2
  • Sara Terryn
    • 3
  • Siew Chiat Cheong
    • 1
    • 2
  • Nicolas Markadieu
    • 4
  • Sylvie Janas
    • 3
  • Marianne Blockmans
    • 1
    • 2
  • Monique Jacoby
    • 1
    • 2
  • Valérie Pouillon
    • 1
    • 2
  • Stéphanie Gayral
    • 1
    • 2
  • Bernard C. Rossier
    • 5
  • Renaud Beauwens
    • 4
  • Christophe Erneux
    • 1
  • Olivier Devuyst
    • 3
    • 6
  • Stéphane Schurmans
    • 1
    • 2
    • 7
    • 8
  1. 1.Institut de Recherches Interdisciplinaires en Biologie Humaine et Moléculaire (IRIBHM)BrusselsBelgium
  2. 2.Institut de Biologie et de Médecine Moléculaires (IBMM)GosseliesBelgium
  3. 3.Division of NephrologyUniversité catholique de Louvain Medical SchoolBrusselsBelgium
  4. 4.Laboratoire de Physiologie Cellulaire et Moléculaire, Faculté de MédecineUniversité Libre de BruxellesBrusselsBelgium
  5. 5.Département de Pharmacologie et de ToxicologieUniversité de LausanneLausanneSwitzerland
  6. 6.Institute of Physiology, Zurich Centre for Integrative Human Physiology (ZIHP)University of ZurichZurichSwitzerland
  7. 7.Laboratoire de Génétique Fonctionnelle, GIGA-Research Centre/B34LiègeBelgium
  8. 8.Secteur de Biochimie Métabolique, Département des Sciences Fonctionnelles, Faculté de Médecine-VétérinaireUniversité de LiègeLiègeBelgium

Personalised recommendations