P.R254Q mutation in the aquaporin-2 water channel causing dominant nephrogenic diabetes insipidus is due to a lack of arginine vasopressin-induced phosphorylation

Human Mutation

Volumn 30, Issue 10, 2009, Pages E891-E903

  Savelkoul, Paul J M ^a   De Mattia, Fabrizio ^a   Li, Yuedan ^a   Kamsteeg, Erik Jan ^a   Konings, Irene B M ^a   van der Sluijs, Peter ^b   Deen, Peter M T ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

AQP2; Membrane trafficking; Phosphorylation; Pka; Water channel

Indexed keywords

AQUAPORIN 2; ARGIPRESSIN; BIOPOLYMER; PRIMER DNA;

ANIMAL; ARTICLE; CELL CULTURE; CELL MEMBRANE; DOG; DOMINANT GENE; GENETICS; HUMAN; METABOLISM; MUTATION; NEPHROGENIC DIABETES INSIPIDUS; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION;

ANIMALS; AQUAPORIN 2; ARGININE VASOPRESSIN; BASE SEQUENCE; BIOPOLYMERS; CELL MEMBRANE; CELLS, CULTURED; DIABETES INSIPIDUS, NEPHROGENIC; DNA PRIMERS; DOGS; GENES, DOMINANT; HUMANS; MUTATION; PHOSPHORYLATION;

EID: 73349112896     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.21082     Document Type: Article

References (42)

1. Asai T, Kuwahara M, Kurihara H, Sakai T, Terada Y, Marumo F, Sasaki S. 2003. Pathogenesis of nephrogenic diabetes insipidus by aquaporin-2 C-terminus mutations. Kidney Int 64:2-10
2. Bao J, Alroy I, Waterman H, Schejter ED, Brodie C, Yarden Y. 2000. Threonine phosphorylation diverts internalized EGF-receptors from a degradative pathway to the recycling endosome. J Biol Chem.
3. Benham AM, Cabibbo A, Fassio A, Bulleid N, Sitia R, Braakman I. 2000. The CXXCXXC motif determines the folding, structure and stability of human Ero1-Lalpha. EMBO J 19:4493-4502
4. Brown D, Weyer P, Orci L. 1988. Vasopressin stimulates endocytosis in kidney collecting duct principal cells. Eur J Cell Biol 46:336-341
5. Christensen BM, Zelenina M, Aperia A, Nielsen S. 2000. Localization and regulation of PKA-phosphorylated AQP2 in response to V(2)-receptor agonist/antagonist treatment. Am J Physiol Renal Physiol 278:F29-F42
6. Christoforidis S, McBride HM, Burgoyne RD, Zerial M. 1999. The Rab5 effector EEA1 is a core component of endosome docking. Nature 397:621-625
7. De Mattia F, Savelkoul PJ, Kamsteeg EJ, Konings IB, van der SP, Mallmann R, Oksche A, Deen PM. 2005. Lack of Arginine Vasopressin-Induced Phosphorylation of Aquaporin-2 Mutant AQP2-R254L Explains Dominant Nephrogenic Diabetes Insipidus. J Am Soc Nephrol 16:2872-2880
8. Deen PMT, Nielsen S, Bindels RJM, van Os CH. 1997a. Apical and basolateral expression of Aquaporin-1 in transfected MDCK and LLC-PK cells and functional evaluation of their transcellular osmotic water permeabilities. Pflugers Arch 433:780-787
9. Deen PMT, Rijss JPL, Mulders SM, Errington RJ, van Baal J, van Os CH. 1997b. Aquaporin-2 transfection of Madin-Darby canine kidney cells reconstitutes vasopressin-regulated transcellular osmotic water transport. Journal of the American Society of Nephrology 8:1493-1501
10. Deen PMT, Van Balkom BWM, Savelkoul PJ, Kamsteeg EJ, Van Raak M, Jennings ML, Muth TR, Rajendran V, Caplan MJ. 2002. Aquaporin-2: COOH terminus is necessary but not sufficient for routing to the apical membrane. Am J Physiol Renal Physiol 282:F330-F340
11. Deen PMT, Verdijk MAJ, Knoers NVAM, Wieringa B, Monnens LAH, van Os CH, van Oost BA. 1994. Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine. Science 264:92-95
12. 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
13. Ghosh RN, Mallet WG, Soe TT, McGraw TE, Maxfield FR. 1998. An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking through the endocytic recycling compartment in CHO cells. J Cell Biol 142:923-936
14. Heilker R, Spiess M, Crottet P. 1999. Recognition of sorting signals by clathrin adaptors. Bioessays 21:558-567
15. Kamsteeg EJ, Bichet DG, Konings IB, Nivet H, Lonergan M, Arthus MF, van Os CH, Deen PMT. 2003. Reversed polarized delivery of an aquaporin-2 mutant causes dominant nephrogenic diabetes insipidus. J Cell Biol 163:1099-1109
16. Kamsteeg EJ, Deen PMT. 2001. Detection of aquaporin-2 in the plasma membranes of oocytes: a novel isolation method with improved yield and purity. Biochem Biophys Res Commun 282:683-690
17. Kamsteeg EJ, Heijnen I, van Os CH, Deen PMT. 2000a. The Subcellular Localization of an Aquaporin-2 Tetramer Depends on the Stoichiometry of Phosphorylated and Nonphosphorylated Monomers. J Cell Biol 151:919-930
18. Kamsteeg EJ, Mulders SM, Bichet DG, Deen PMT, van Os C. 2000b. Consequences of aquaporin 2 tetramerization for genetics and routing. Nephrol Dial Transplant 15 Suppl 6:26-28
19. Kamsteeg EJ, Wormhoudt TA, Rijss JPL, van Os CH, Deen PMT. 1999. An impaired routing of wild-type aquaporin-2 after tetramerization with an aquaporin-2 mutant explains dominant nephrogenic diabetes insipidus. EMBO J 18:2394-2400
20. Katsura T, Gustafson CE, Ausiello DA, Brown D. 1997. Protein kinase A phosphorylation is involved in regulated exocytosis of aquaporin-2 in transfected LLC-PK1 cells. Am J Physiol 41:F816-F822
21. Kuwahara M, Iwai K, Ooeda T, Igarashi T, Ogawa E, Katsushima Y, Shinbo I, Uchida S, Terada Y, Arthus MF, Lonergan M, Fujiwara TM, Bichet DG, Marumo F, Sasaki S. 2001. Three families with autosomal dominant nephrogenic diabetes insipidus caused by aquaporin-2 mutations in the C-terminus. Am J Hum Genet 69:738-748
22. Lu H, Sun TX, Bouley R, Blackburn K, McLaughlin M, Brown D. 2003. Inhibition of endocytosis causes phosphorylation (S256)-independent plasma membrane accumulation of AQP-2. Am J Physiol Renal Physiol
23. Marr N, Bichet DG, Hoefs S, Savelkoul PJ, Konings IB, De Mattia F, Graat MP, Arthus MF, Lonergan M, Fujiwara TM, Knoers NVAM, Landau D, Balfe WJ, Oksche A, Rosenthal W, Muller D, van Os CH, Deen PMT. 2002a. Cell-Biologic and Functional Analyses of Five New Aquaporin-2 Missense Mutations that Cause Recessive Nephrogenic Diabetes Insipidus. J Am Soc Nephrol 13:2267-2277
24. Marr N, Bichet DG, Lonergan M, Arthus MF, Jeck N, Seyberth HW, Rosenthal W, van Os CH, Oksche A, Deen PMT. 2002b. Heteroligomerization of an Aquaporin-2 mutant with wild-type Aquaporin- 2 and their misrouting to late endosomes/lysosomes explains dominant nephrogenic diabetes insipidus. Hum Mol Genet 11:779-789
25. McDill BW, Li SZ, Kovach PA, Ding L, Chen F. 2006. Congenital progressive hydronephrosis (cph) is caused by an S256L mutation in aquaporin-2 that affects its phosphorylation and apical membrane accumulation. Proc Natl Acad Sci U S A 103:6952-6957
26. Molloy SS, Anderson ED, Jean F, Thomas G. 1999. Bi-cycling the furin pathway: from TGN localization to pathogen activation and embryogenesis. Trends Cell Biol 9:28-35
27. Mulders SM, Bichet DG, Rijss JPL, Kamsteeg EJ, Arthus MF, Lonergan M, Fujiwara M, Morgan K, Leijendekker R, van der Sluijs P, van Os CH, Deen PMT. 1998. An aquaporin-2 water channel mutant which causes autosomal dominant nephrogenic diabetes insipidus is retained in the Golgi complex. J Clin Invest 102:57-66
28. Nielsen S, Chou CL, Marples D, Christensen EI, Kishore BK, Knepper MA. 1995. Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci U S A 92:1013-1017
29. Nielsen S, Digiovanni SR, Christensen EI, Knepper MA, Harris HW. 1993. Cellular and subcellular immunolocalization of vasopressin- regulated water channel in rat kidney. Proc Natl Acad Sci U S A 90:11663-11667
30. Nishimoto G, Zelenina M, Li D, Yasui M, Aperia A, Nielsen S, Nairn AC. 1999. Arginine vasopressin stimulates phosphorylation of aquaporin-2 in rat renal tissue. Am J Physiol 276:F254-F259
31. Robben JH, Knoers NV, Deen PM. 2006. Cell biological aspects of the vasopressin type-2 receptor and aquaporin 2 water channel in nephrogenic diabetes insipidus. Am J Physiol Renal Physiol 291:F257-F270
32. Robertson GL, Kopp P. 2002. A novel dominant mutation of the aquaporin-2 gene resulting in partial nephrogenic diabetes insipidus
33. Rohn WM, Rouille Y, Waguri S, Hoflack B. 2000. Bi-directional trafficking between the trans-Golgi network and the endosomal/lysosomal system. J Cell Sci 113 (Pt 12):2093-2101
34. Rosenthal W, Seibold A, Antaramian A, Lonergan M, Arthus M-F, Hendy GN, Birnbaumer M, Bichet DG. 1992. Molecular identification of the gene responsible for congenital nephrogenic diabetes insipidus. Nature 359:233-235
35. Sonnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M. 2000. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 149:901-914
36. Strange K, Willingham MC, Handler JS, Harris HW, Jr. 1988. Apical membrane endocytosis via coated pits is stimulated by removal of antidiuretic hormone from isolated, perfused rabbit cortical collecting tubule. J Membr Biol 103:17-28
37. Sun TX, van Hoek A, Huang Y, Bouley R, McLaughlin M, Brown D. 2002. Aquaporin-2 localization in clathrin-coated pits: inhibition of endocytosis by dominant-negative dynamin. Am J Physiol Renal Physiol 282:F998-1011
38. Van Balkom BWM, Savelkoul PJ, markovich D, Hofman E, Nielsen S, van der Sluijs P, Deen PMT. 2002. The role of putative phosphorylation sites in the targeting and shuttling of the aquaporin-2 water channel. J Biol Chem 277:41473-41479
39. van den Ouweland AM, Dreesen JC, Verdijk MAJ, Knoers NVAM. 1992. Mutations in the vasopressin type 2 receptor gene (AVPR2) associated with Nephrogenic Diabetes Insipidus. Nat Genet 2:99-102
40. van Os CH, Deen PMT. 1998. Aquaporin-2 water channel mutations causing nephrogenic diabetes insipidus. Proc Assoc Am Physicians 110:395-400
41. van Os CH, Deen PMT, Dempster JA. 1994. Aquaporins: water selective channels in biological membranes. Molecular structure and tissue distribution. Biochim Biophys Acta 1197:291-309
42. Wade JB, Stetson DL, Lewis SA. 1981. ADH action: evidence for a membrane shuttle mechanism. Ann N Y Acad Sci 372:106-117