Bilateral ureteral obstruction induces early downregulation and redistribution of AQP2 and phosphorylated AQP2

American Journal of Physiology - Renal Physiology

Volumn 301, Issue 1, 2011, Pages

  Stødkilde, Lene ^a   Nørregaard, Rikke ^a   Fenton, Robert A ^a   Wang, Guixian ^a   Knepper, Mark A ^b   Frøkiær, Jørgen ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Degradation; Membrane protein; Urine concentrating capacity; Water transport

Indexed keywords

AQUAPORIN 2; SODIUM CHLORIDE; WATER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILATERAL URETER OBSTRUCTION; CONTROLLED STUDY; DOWN REGULATION; ENDOSOME; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LYSOSOME; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; URETER OBSTRUCTION;

EID: 79960069131     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00664.2010     Document Type: Article

References (43)

1. Bouley R, Hawthorn G, Russo LM, Lin HY, Ausiello DA, Brown D. Aquaporin 2 (AQP2) and vasopressin type 2 receptor (V2R) endocytosis in kidney epithelial cells: AQP2 is located in 'endocytosis-resistant' membrane domains after vasopressin treatment. Biol Cell 98: 215-232, 2006.
2. Chen G, Huang H, Frohlich O, Yang Y, Klein JD, Price SR, Sands JM. MDM2 E3 ubiquitin ligase mediates UT-A1 urea transporter ubiquitination and degradation. Am J Physiol Renal Physiol 295: F1528-F1534, 2008.
3. Christensen BM, Zelenina M, Aperia A, Nielsen S. Localization and regulation of PKA-phosphorylated AQP2 in response to V2-receptor agonist/antagonist treatment. Am J Physiol Renal Physiol 278: F29-F42, 2000.
4. DiGiovanni SR, Nielsen S, Christensen EI, Knepper MA. Regulation of collecting duct water channel expression by vasopressin in Brattleboro rat. Proc Natl Acad Sci USA 91: 8984-8988, 1994.
5. Edwards RM, Jackson BA, Dousa TP. ADH-sensitive cAMP system in papillary collecting duct: effect of osmolality and PGE2. Am J Physiol Renal Fluid Electrolyte Physiol 240: F311-F318, 1981.
6. Eto K, Noda Y, Horikawa S, Uchida S, Sasaki S. Phosphorylation of aquaporin-2 regulates its water permeability. J Biol Chem 285: 40777-40784, 2010.
7. Fenton RA, Brond L, Nielsen S, Praetorius J. Cellular and subcellular distribution of the type-2 vasopressin receptor in the kidney. Am J Physiol Renal Physiol 293: F748-F760, 2007.
8. Fenton RA, Moeller HB, Hoffert JD, Yu MJ, Nielsen S, Knepper MA. Acute regulation of aquaporin-2 phosphorylation at Ser-264 by vasopressin. Proc Natl Acad Sci USA 105: 3134-3139, 2008.
9. Frøkiær J, Christensen BM, Marples D, Djurhuus JC, Jensen UB, Knepper MA, Nielsen S. Downregulation of aquaporin-2 parallels changes in renal water excretion in unilateral ureteral obstruction. Am J Physiol Renal Physiol 273: F213-F223, 1997.
10. Frøkiær J, Marples D, Knepper M, Nielsen S. Bilateral ureteral obstruction downregulates expression of the vasopressin sensitive aquaporin-2 water channel in rat kidney. Am J Physiol Renal Fluid Electrolyte Physiol 270: F657-F668, 1996.
11. Fushimi K, Sasaki S, Marumo F. Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of the aquaporin-2 water channel. J Biol Chem 272: 14800-14804, 1997.
12. Hasler U, Nielsen S, Feraille E, Martin PY. Posttranscriptional control of aquaporin-2 abundance by vasopressin in renal collecting duct principal cells. Am J Physiol Renal Physiol 290: F177-F187, 2006.
13. Hayashi M, Sasaki S, Tsuganezawa H, Monkawa T, Kitajima W, Konishi K, Fushimi K, Marumo F, Saruta T. Role of vasopressin V2 receptor in acute regulation of aquaporin-2. Kidney Blood Press Res 19: 32-37, 1996.
14. Hendriks G, Koudijs M, van Balkom BW, Oorschot V, Klumperman J, Deen PM, van der Sluijs P. Glycosylation is important for cell surface expression of the water channel aquaporin-2 but is not essential for tetramerization in the endoplasmic reticulum. J Biol Chem 279: 2975-2983, 2004.
15. Hoffert JD, Fenton RA, Moeller HB, Simons B, Tchapyjnikov D, McDill BW, Yu MJ, Pistikun T, Chen F, Knepper MA. Vasopressinstimulated increase in phosphorylation at Ser269 potentiates plasma membrane retention of aquaporin-2. J Biol Chem 283: 24617-24627, 2008.
16. Hoffert JD, Nielsen J, Yu MJ, Pisitkun T, Schleicher SM, Nielsen S, Knepper MA. Dynamics of aquaporin-2 serine-261 phosphorylation in response to short-term vasopressin treatment in collecting duct. Am J Physiol Renal Physiol 292: F691-F700, 2007.
17. Hoffert JD, Pisitkun T, Wang G, Shen RF, Knepper MA. Quantitative phosphoproteomics of vasopressin-sensitive renal cells: regulation of aquaporin-2 phosphorylation at two sites. Proc Natl Acad Sci USA 103: 7159-7164, 2006.
18. Jensen AM, Bae EH, Fenton RA, Nørregaard R, Nielsen S, Kim SW, Frøkiær J. Angiotensin II regulates V2 receptor and pAQP2 during ureteral obstruction. Am J Physiol Renal Physiol 296: F127-F134, 2009.
19. Kamsteeg EJ, Hendriks G, Boone M, Konings IB, Oorschot V, van der Sluijs P, Klumperman J, Deen PM. Short-chain ubiquitination mediates the regulated endocytosis of the aquaporin-2 water channel. Proc Natl Acad Sci USA 103: 18344-18349, 2006.
20. Katsura T, Ausiello DA, Brown D. Direct demonstration of aquaporin-2 water channel recycling in stably transfected LLC-PK1 epithelial cells. Am J Physiol Renal Fluid Electrolyte Physiol 270: F548-F553, 1996.
21. Katsura T, Gustafson CE, Ausiello DA, Brown D. Protein kinase A phosphorylation is involved in regulated exocytosis of aquaporin-2 in transfected LLC-PK1 cells. Am J Physiol Renal Physiol 272: F817-F822, 1997.
22. Klahr S, Harris K, Purkerson ML. Effects of obstruction on renal functions. Pediatr Nephrol 2: 34-42, 1988.
23. Kurokawa K, Massry SG. Interaction between catecholamines and vasopressin on renal medullary cyclic AMP of rat. Am J Physiol 225: 825-829, 1973.
24. Li C, Wang W, Knepper MA, Nielsen S, Frøkiær J. Downregulation of renal aquaporins in response to unilateral ureteral obstruction. Am J Physiol Renal Physiol 284: F1066-F1079, 2003.
25. Li C, Wang W, Kwon TH, Isikay L, Wen JG, Marples D, Djurhuus JC, Stockwell A, Knepper MA, Nielsen S, Frøkiær J. Downregulation of AQP1, _2, and _3 after ureteral obstruction is associated with a long-term urine-concentrating defect. Am J Physiol Renal Physiol 281: F163-F171, 2001.
26. Lu H, Sun TX, Bouley R, Blackburn K, McLaughlin M, Brown D. Inhibition of endocytosis causes phosphorylation (S256)-independent plasma membrane accumulation of AQP2. Am J Physiol Renal Physiol 286: F233-F243, 2004.
27. Lu HJ, Matsuzaki T, Bouley R, Hasler U, Qin QH, Brown D. The phosphorylation state of serine 256 is dominant over that of serine 261 in the regulation of AQP2 trafficking in renal epithelial cells. Am J Physiol Renal Physiol 295: F290-F294, 2008.
28. Matsumura Y, Uchida S, Rai T, Sasaki S, Marumo F. Transcriptional regulation of aquaporin-2 water channel gene by cAMP. J Am Soc Nephrol 8: 861-867, 1997.
29. McDill BW, Li SZ, Kovach PA, Ding L, Chen F. 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 USA 103: 6952-6957, 2006.
30. Mellman I. Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 12: 575-625, 1996.
31. Moeller HB, MacAulay N, Knepper MA, Fenton RA. Role of multiple phosphorylation sites in the COOH-terminal tail of aquaporin-2 for water transport: evidence against channel gating. Am J Physiol Renal Physiol 296: F649-F657, 2009.
32. Moeller HB, Praetorius J, Rutzler MR, Fenton RA. Phosphorylation of aquaporin-2 regulates its endocytosis and protein-protein interactions. Proc Natl Acad Sci USA 107: 424-429, 2009.
33. Nielsen S, Chou CL, Marples D, Christensen EI, Kishore BK, Knepper MA. Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci USA 92: 1013-1017, 1995.
34. Nishimoto G, Zelenina M, Li D, Yasui M, Aperia A, Nielsen S, Nairn AC. Arginine vasopressin stimulates phosphorylation of aquaporin-2 in rat renal tissue. Am J Physiol Renal Physiol 276: F254-F259, 1999.
35. Nørregaard R, Jensen BL, Topcu SO, Diget M, Schweer H, Knepper MA, Nielsen S, Frøkiær J. COX-2 activity transiently contributes to increased water and NaCl excretion in the polyuric phase after release of ureteral obstruction. Am J Physiol Renal Physiol 292: F1322-F1333, 2007.
36. Nørregaard R, Jensen BL, Topcu SO, Wang G, Schweer H, Nielsen S, Frøkiær J. Urinary tract obstruction induces transient accumulation of COX-2-derived prostanoids in kidney tissue. Am J Physiol Regul Integr Comp Physiol 298: R1017-R1025, 2010.
37. Pisitkun T, Shen RF, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci USA 101: 13368-13373, 2004.
38. Reyes AA, Robertson G, Klahr S. Role of vasopressin in rats with bilateral ureteral obstruction. Proc Soc Exp Biol Med 197: 49-55, 1991.
39. Rosenthal W, Antaramian A, Gilbert S, Birnbaumer M. Nephrogenic diabetes insipidus. A V2 vasopressin receptor unable to stimulate adenylyl cyclase. J Biol Chem 268: 13030-13033, 1993.
40. Tajika Y, Matsuzaki T, Suzuki T, Aoki T, Hagiwara H, Kuwahara M, Sasaki S, Takata K. Aquaporin-2 is retrieved to the apical storage compartment via early endosomes and phosphatidylinositol 3-kinasedependent pathway. Endocrinology 145: 4375-4383, 2004.
41. Tamma G, Robben JH, Trimpert C, Boone M, Deen PM. Regulation of AQP2 localization by S256 and S261 phosphorylation and ubiquitination. Am J Physiol Cell Physiol 300: C636-C646, 2011.
42. Valenti G, Procino G, Carmosino M, Frigeri A, Mannucci R, Nicoletti I, Svelto M. The phosphatase inhibitor okadaic acid induces AQP2 translocation independently from AQP2 phosphorylation in renal collecting duct cells. J Cell Sci 113: 1985-1992, 2000.
43. van Balkom BW, Savelkoul PJ, Markovich D, Hofman E, Nielsen S, van der Sluijs P, Deen PM. The role of putative phosphorylation sites in the targeting and shuttling of the aquaporin-2 water channel. J Biol Chem 277: 41473-41479, 2002.