Reciprocal regulation of aquaporin-2 abundance and degradation by protein kinase A and p38-MAP kinase

Journal of the American Society of Nephrology

Volumn 21, Issue 10, 2010, Pages 1645-1656

  Nedvetsky, Pavel I ^a   Tabor, Vedrana ^a   Tamma, Grazia ^b   Beulshausen, Sven ^a   Skroblin, Philipp ^a   Kirschner, Aline ^a   Mutig, Kerim ^c   Boltzen, Mareike ^a   Petrucci, Oscar ^a   Vossenkämper, Anna ^a   Wiesner, Burkhard ^a   Bachmann, Sebastian ^c   Rosenthal, Walter ^c,d   Klussmann, Enno ^a  

^a LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^b UNIVERSITY OF BARI   (Italy)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN 2; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; ARGIPRESSIN; FORSKOLIN; PROTEASOME;

ARTICLE; CELL MEMBRANE PERMEABILITY; CELL STRAIN HEK293; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; KIDNEY COLLECTING TUBULE; KIDNEY MEDULLA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; TRANSLATION INITIATION; UBIQUITINATION; ANIMAL; C57BL MOUSE; CELL LINE; GENETIC TRANSCRIPTION; METABOLISM; MOUSE; PHOSPHORYLATION; PROTEIN SYNTHESIS; RAT;

ANIMALS; AQUAPORIN 2; ARGININE VASOPRESSIN; CELL LINE; COLFORSIN; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HUMANS; KIDNEY MEDULLA; KIDNEY TUBULES, COLLECTING; MICE; MICE, INBRED C57BL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BIOSYNTHESIS; RATS; TRANSCRIPTION, GENETIC;

EID: 77957879635     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2009111190     Document Type: Article

References (39)

1. Fushimi K, Uchida S, Hara Y, Hirata Y, Marumo F, Sasaki S: Cloning and expression of apical membrane water channel of rat kidney collecting tubule. Nature 361: 549-552, 1993
2. 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
3. King LS, Kozono D, Agre P: From structure to disease: The evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 5: 687-698, 2004
4. Nedvetsky PI, Tamma G, Beulshausen S, Valenti G, Rosenthal W, Klussmann E: Regulation of aquaporin-2 trafficking. Handb Exp Pharmacol (190): 133-157, 2009
5. Yasui M, Zelenin SM, Celsi G, Aperia A: Adenylate cyclase-coupled vasopressin receptor activates AQP2 promoter via a dual effect on CRE and AP1 elements. Am J Physiol 272: F443-F450, 1997
6. 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
7. Hasler U, Mordasini D, Bens M, Bianchi M, Cluzeaud F, Rousselot M, Vandewalle A, Feraille E, Martin PY: Long term regulation of aquaporin-2 expression in vasopressin-responsive renal collecting duct principal cells. J Biol Chem 277: 10379-10386, 2002 (Pubitemid 34968157)
8. Puliyanda DP, Ward DT, Baum MA, Hammond TG, Harris, HW Jr: Calpain-mediated AQP2 proteolysis in inner medullary collecting duct. Biochem Biophys Res Commun 303: 52-58, 2003
9. Woelk T, Oldrini B, Maspero E, Confalonieri S, Cavallaro E, Di Fiore PP, Polo S: Molecular mechanisms of coupled monoubiquitination. Nat Cell Biol 8: 1246-1254, 2006
10. 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 U S A 103: 18344-18349, 2006
11. van Balkom BW, Boone M, Hendriks G, Kamsteeg EJ, Robben JH, Stronks HC, van der Voorde A, van Herp F, van der Sluijs P, Deen PM: LIP5 interacts with aquaporin 2 and facilitates its lysosomal degradation. J Am Soc Nephrol 20: 990-1001, 2009
12. 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 U S A 105: 3134-3139, 2008
13. Hoffert JD, Fenton RA, Moeller HB, Simons B, Tchapyjnikov D, McDill BW, Yu MJ, Pisitkun T, Chen F, Knepper MA: Vasopressin-stimulated increase in phosphorylation at Ser269 potentiates plasma membrane retention of aquaporin-2. J Biol Chem 283: 24617-24627, 2008
14. Moeller HB, Knepper MA, Fenton RA: Serine 269 phosphorylated aquaporin-2 is targeted to the apical membrane of collecting duct principal cells. Kidney Int 75: 295-303, 2009
15. 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 U S A 103: 7159-7164, 2006
16. Rinschen MM, Yu MJ, Wang G, Boja ES, Hoffert JD, Pisitkun T, Knepper MA: Quantitative phosphoproteomic analysis reveals vasopressin V2-receptor-dependent signaling pathways in renal collecting duct cells. Proc Natl Acad Sci U S A 107: 3882-3887, 2010
17. Zhang B, Bui TN, Xiang J, Lin A: Cyclic AMP inhibits p38 activation via CREB-induced dynein light chain. Mol Cell Biol 4: 1223-1224, 2006
18. Gianni M, Parrella E, Raska I Jr, Gaillard E, Nigro EA, Gaudon C, Garattini E, Rochette-Egly C: P38MAPK-dependent phosphorylation and degradation of SRC-3/AIB1 and RARalpha-mediated transcription. EMBO J 25: 739-751, 2006
19. Maric K, Oksche A, Rosenthal W: Aquaporin-2 expression in primary cultured rat inner medullary collecting duct cells. Am J Physiol 275: F796-F801, 1998
20. Stefan E, Wiesner B, Baillie GS, Mollajew R, Henn V, Lorenz D, Furkert J, Santamaria K, Nedvetsky P, Hundsrucker C, Beyermann M, Krause E, Pohl P, Gall I, MacIntyre AN, Bachmann S, Houslay MD, Rosenthal W, Klussmann E: Compartmentalization of cAMP-dependent signaling by phosphodiesterase-4D is involved in the regulation of vasopressin-mediated water reabsorption in renal principal cells. J Am Soc Nephrol 18: 199-212, 2007
21. Nedvetsky PI, Stefan E, Frische S, Santamaria K, Wiesner B, Valenti G, Hammer JA 3rd, Nielsen S, Goldenring JR, Rosenthal W, Klussmann E: A role of myosin Vb and Rab11-FIP2 in the aquaporin-2 shuttle. Traffic 8: 110-123, 2007
22. 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
23. Katsura T, Ausiello DA, Brown D: Direct demonstration of aquaporin-2 water channel recycling in stably transfected LLC-PK1 epithelial cells. Am J Physiol 270: F548-F553, 1996
24. Terris J, Ecelbarger CA, Nielsen S, Knepper MA: Long-term regulation of four renal aquaporins in rats. Am J Physiol 271: F414-F422, 1996
25. Tajika Y, Matsuzaki T, Suzuki T, Ablimit A, Aoki T, Hagiwara H, Kuwahara M, Sasaki S, Takata K: Differential regulation of AQP2 trafficking in endosomes by microtubules and actin filaments. Histochem Cell Biol 124: 1-12, 2005
26. 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 272: F817-F822, 1997
27. 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
28. 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
29. Casanovas O, Jaumot M, Paules AB, Agell N, Bachs O: P38SAPK2 phosphorylates cyclin D3 at Thr-283 and targets it for proteasomal degradation. Oncogene 23: 7537-7544, 2004
30. Uchida S, Yoshioka K, Kizu R, Nakagama H, Matsunaga T, Ishizaka Y, Poon RY, Yamashita K: Stress-activated mitogen-activated protein kinases c-Jun NH2-terminal kinase and p38 target Cdc25B for degradation. Cancer Res 69: 6438-6444, 2009
31. Li W, Ye Y: Polyubiquitin chains: Functions, structures, and mechanisms. Cell Mol Life Sci 65: 2397-2406, 2008
32. Welchman RL, Gordon C, Mayer RJ: Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat Rev Mol Cell Biol 6: 599-609, 2005
33. 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
34. Lorenz D, Krylov A, Hahm D, Hagen V, Rosenthal W, Pohl P, Maric K: Cyclic AMP is sufficient for triggering the exocytic recruitment of aquaporin-2 in renal epithelial cells. EMBO Rep 4: 88-93, 2003
35. 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
36. Liebenhoff U, Rosenthal W: Identification of Rab3-, Rab5a- and synaptobrevin II-like proteins in a preparation of rat kidney vesicles containing the vasopressin-regulated water channel. FEBS Lett 365: 209-213, 1995
37. Bieche I, Olivi M, Champeme MH, Vidaud D, Lidereau R, Vidaud M: Novel approach to quantitative polymerase chain reaction using real-time detection: application to the detection of gene amplification in breast cancer. Int J Cancer 78: 661-666, 1998
38. Mutig K, Paliege A, Kahl T, Jons T, Muller-Esterl W, Bachmann S: Vasopressin V2 receptor expression along rat, mouse, and human renal epithelia with focus on TAL. Am J Physiol Renal Physiol 293: F1166-F1177, 2007
39. Alken M, Rutz C, Kochl R, Donalies U, Oueslati M, Furkert J, Wietfeld D, Hermosilla R, Scholz A, Beyermann M, Rosenthal W, Schulein R: The signal peptide of the rat corticotropin-releasing factor receptor 1 promotes receptor expression but is not essential for establishing a functional receptor. Biochem J 390: 455-464, 2005