Ser-256 phosphorylation dynamics of aquaporin 2 during maturation from the endoplasmic reticulum to the vesicular compartment in renal cells

FASEB Journal

Volumn 17, Issue 13, 2003, Pages 1-24

  Procino, Giuseppe ^a   Carmosino, Monica ^a   Marin, Oriano ^b   Brunanti, Anna M ^b   Contri, Antonella ^b   Pinna, Lorenzo A ^b   Mannucci, Roberta ^c   Nielsen, Soren ^d   Kwon, Tae Hwan ^e   Svelto, Maria ^a   Valenti, Giovanna ^a  

^a UNIVERSITY OF BARI   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c UNIVERSITY OF PERUGIA   (Italy)

^d AARHUS UNIVERSITY   (Denmark)

^e Dongguk University College of Medicine   (South Korea)

Author keywords

Golgi casein kinase; NDI; Phosphorylation; PKA

Indexed keywords

EID: 84875058225     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.02-0870fje     Document Type: Article

References (42)

1. Katsura, T., Gustafson, C. E., Ausiello, D. A., and Brown, D. (1997) Protein kinase A phosphorylation is involved in regulated exocytosis of aquaporin-2 in transfected LLC-PK1 cells. Am. J. Physiol. 272, F817-F822
2. Fushimi, K., Sasaki, S., and 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 (Pubitemid 27251748)
3. Nishimoto, G., Zelenina, M., Li, D., Yasui, M., Aperia, A., Nielsen, S., and Nairn, A. C. (1999) Arginine vasopressin stimulates phosphorylation of aquaporin-2 in rat renal tissue. Am. J. Physiol. 276, F254-F259 (Pubitemid 29102290)
4. Christensen, B. M., Zelenina, M., Aperia, A., and Nielsen, S. (2000) Localization and regulation of PKA-phosphorylated AQP2 in response to V2-receptor agonist/antagonist treatment. Am. J. Physiol. 278, F29-F42 (Pubitemid 30106123)
5. Kamsteeg, E. J., Heijnen, I., van Os, C. H., and Deen, P. M. (2000) The Subcellular Localization of an Aquaporin-2 Tetramer Depends on the Stoichiometry of Phosphorylated and Nonphosphorylated Monomers. J. Cell Biol. 151, 919-930
6. Simon, J. P., Ivanov, I. E., Shopsin, B., Hersh, D., Adesnik, M., and Sabatini, D. D. (1996) The in vitro generation of post-Golgi vesicles carrying viral envelope glycoproteins requires an ARF-like GTP-binding protein and a protein kinase C associated with the Golgi apparatus. J. Biol. Chem. 271, 16952-16961 (Pubitemid 26239067)
7. Jones, S. M., Alb, J. G., Jr., Phillips, S. E., Bankaitis, V. A., and Howell, K. E. (1998) A phosphatidylinositol 3-kinase and phosphatidylinositol transfer protein act synergistically in formation of constitutive transport vesicles from the trans-Golgi network. J. Biol. Chem. 273, 10349-10354 (Pubitemid 28227641)
8. Molloy, S. S., Thomas, L., Kamibayashi, C., Mumby, M. C., and Thomas, G. (1998) Regulation of endosome sorting by a specific PP2A isoform. J. Cell Biol. 142, 1399-1411 (Pubitemid 28452592)
9. Muniz, M., Martin, M. E., Hidalgo, J., and Velasco, A. (1997) Protein kinase A activity is required for the budding of constitutive transport vesicles from the trans-Golgi network. Proc. Natl. Acad. Sci. USA 94, 14461-14466 (Pubitemid 28041396)
10. Martin, M. E., Hidalgo, J., Rosa, J. L., Crottet, P., and Velasco, A. (2000) Effect of protein kinase A activity on the association of ADP-ribosylation factor 1 to golgi membranes. J. Biol. Chem. 275, 19050-19059 (Pubitemid 30422872)
11. Lande, M. B., Jo, I., Zeidel, M. L., Somers, M., and Harris, H. W., Jr. (1996) Phosphorylation of aquaporin-2 does not alter the membrane water permeability of rat papillary water channel-containing vesicles. J. Biol. Chem. 271, 5552-5557 (Pubitemid 26083886)
12. Valenti, G., Procino, G., Carmosino, M., Frigeri, A., Mannucci, R., Nicoletti, I., and Svelto, M. (2000) The phosphatase inhibitor okadaic acid induces AQP2 translocation independently from AQP2 phosphorylation in renal collecting duct cells. J. Cell Sci. 113, 1985-1992 (Pubitemid 30386502)
13. Valenti, G., Frigeri, A., Ronco, P. M., D'Ettorre, C., and Svelto, M. (1996) Expression and functional analysis of water channels in a stably AQP2- transfected human collecting duct cell line. J. Biol. Chem. 271, 24365-24370 (Pubitemid 26333167)
14. Pelham, H. R. (1991) Multiple targets for brefeldin A. Cell 67, 449-451
15. Sciaky, N., Presley, J., Smith, C., Zaal, K. J., Cole, N., Moreira, J. E., Terasaki, M., Siggia, E., and Lippincott-Schwartz, J. (1997) Golgi tubule traffic and the effects of brefeldin A visualized in living cells. J. Cell Biol. 139, 1137-1155 (Pubitemid 27523203)
16. Chardin, P., and McCormick, F. (1999) Brefeldin A: the advantage of being uncompetitive. Cell 97, 153-155 (Pubitemid 29194265)
17. Tamarappoo, B. K., Yang, B., and Verkman, A. S. (1999) Misfolding of mutant aquaporin-2 water channels in nephrogenic diabetes insipidus. J. Biol. Chem. 274, 34825-34831 (Pubitemid 129509527)
18. Pagano, R. E., Sepanski, M. A., and Martin, O. C. (1989) Molecular trapping of a fluorescent ceramide analogue at the Golgi apparatus of fixed cells: interaction with endogenous lipids provides a trans-Golgi marker for both light and electron microscopy. J. Cell Biol. 109, 2067-2079 (Pubitemid 19282595)
19. Pinna, L. A., and Ruzzene, M. (1996) How do protein kinases recognize their substrates? Biochim. Biophys. Acta 1314, 191-225
20. Meggio, F., Boulton, A. P., Marchiori, F., Borin, G., Lennon, D. P., Calderan, A., and Pinna, L. A. (1988) Substrate-specificity determinants for a membrane-bound casein kinase of lactating mammary gland. A study with synthetic peptides. Eur. J. Biochem. 177, 281-284
21. Lasa-Benito, M., Marin, O., Meggio, F., and Pinna, L. A. (1996) Golgi apparatus mammary gland casein kinase: monitoring by a specific peptide substrate and definition of specificity determinants. FEBS Lett. 382, 149-152 (Pubitemid 26092246)
22. Lasa, M., Marin, O., and Pinna, L. A. (1997) Rat liver Golgi apparatus contains a protein kinase similar to the casein kinase of lactating mammary gland. Eur. J. Biochem. 243, 719-725 (Pubitemid 27073440)
23. Mulders, S. M., Bichet, D. G., Rijss, J. P., Kamsteeg, E. J., Arthus, M. F., Lonergan, M., Fujiwara, M., Morgan, K., Leijendekker, R., van der Sluijs, P., et al. (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 (Pubitemid 28323830)
24. Kamsteeg, E. J., Wormhoudt, T. A., Rijss, J. P., van Os, C. H., and Deen, P. M. (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 (Pubitemid 29213273)
25. Vandewalle, A., Lelongt, B., Geniteau-Legendre, M., Baudouin, B., Antoine, M., Estrade, S., Chatelet, F., Verroust, P., Cassingena, R., and Ronco, P. (1989) Maintenance of proximal and distal cell functions in SV40-transformed tubular cell lines derived from rabbit kidney cortex. J. Cell. Physiol. 141, 203-221 (Pubitemid 19243628)
26. Nabi, I. R., Le Bivic, A., Fambrough, D., and Rodriguez-Boulan, E. (1991) An endogenous MDCK lysosomal membrane glycoprotein is targeted basolaterally before delivery to lysosomes. J. Cell Biol. 115, 1573-1584 (Pubitemid 21909997)
27. Tamma, G., Klussmann, E., Procino, G., Svelto, M., Rosenthal, W., and Valenti, G. (2003) cAMP induced AQP2 translocation is associated with RhoA inhibition through RhoA phosphorylation and interaction with RhoGDI. J. Cell Sci. 116, 1519-1525. (Pubitemid 36527498)
28. Van Balkom, B. W., Savelkoul, P. J., Markovich, D., Hofman, E., Nielsen, S., Van Der Sluijs, P., and Deen, P. M. (2002) The role of putative phosphorylation sites in the targeting and shuttling of the Aquaporin-2 water channel. J. Biol. Chem. 277, 41473-41479. (Pubitemid 35257449)
29. Perkel, V. S., Miura, Y., and Magner, J. A. (1989) Brefeldin A inhibits oligosaccharide processing of glycoproteins in mouse hypothyroid pituitary tissue at several subcellular sites. Proc. Soc. Exp. Biol. Med. 190, 286-293 (Pubitemid 19082224)
30. Donaldson, J. G., and Lippincott-Schwartz, J. (2000) Sorting and signaling at the Golgi complex. Cell 101, 693-696
31. Price, P. A., Rice, J. S., and Williamson, M. K. (1994) Conserved phosphorylation of serines in the Ser-X-Glu/Ser(P) sequences of the vitamin K-dependent matrix Gla protein from shark, lamb, rat, cow, and human. Protein Sci. 3, 822-830 (Pubitemid 24139907)
32. Kennelly, P. J., and Krebs, E. G. (1991) Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J. Biol. Chem. 266, 15555-15558 (Pubitemid 21907685)
33. Hirano, K., Roth, J., Zuber, C., and Ziak, M. (2002) Expression of a mutant ER-retained polytope membrane protein in cultured rat hepatocytes results in Mallory body formation. Histochem. Cell Biol. 117, 41-53 (Pubitemid 34507533)
34. Klussmann, E., Maric, K., Wiesner, B., Beyermann, M., and Rosenthal, W. (1999) Protein kinase A anchoring proteins are required for vasopressin- mediated translocation of aquaporin-2 into cell membranes of renal principal cells. J. Biol. Chem. 274, 4934-4938
35. Okamoto, C. T., Song, W., Bomsel, M., and Mostov, K. E. (1994) Rapid internalization of the polymeric immunoglobulin receptor requires phosphorylated serine 726. J. Biol. Chem. 269, 15676-15682 (Pubitemid 24202160)
36. Orzech, E., Cohen, S., Weiss, A., and Aroeti, B. (2000) Interactions between the exocytic and endocytic pathways in polarized Madin-Darby canine kidney cells. J. Biol. Chem. 275, 15207-15219 (Pubitemid 30337245)
37. Leffers, H., Madsen, P., Rasmussen, H. H., Honore, B., Andersen, A. H., Walbum, E., Vandekerckhove, J., and Celis, J. E. (1993) Molecular cloning and expression of the transformation sensitive epithelial marker stratifin. A member of a protein family that has been involved in the protein kinase C signalling pathway. J. Mol. Biol. 231, 982-998 (Pubitemid 23209874)
38. Fiedler, K., Kellner, R., and Simons, K. (1997) Mapping the protein composition of trans- Golgi network (TGN)-derived carrier vesicles from polarized MDCK cells. Electrophoresis 18, 2613-2619 (Pubitemid 28133343)
39. de Mattia, F., Savelkoul, P. W. M., Nielsen, S., Oksche, A., and Deen, P. M. T. (2002) An impaired routing of wild-type aquaporin-2/AQP2-R254L complexes explains dominant nephrogenic diabetes insipidus, but is independent from AQP2 phosphorylation. In ASN 35th Annual Meeting, Pennsylvania Convention Center, Philadelphia, PA
40. Brunati, A. M., Contri, A., Muenchbach, M., James, P., Marin, O., and Pinna, L. A. (2000) GRP94 (endoplasmin) co-purifies with and is phosphorylated by Golgi apparatus casein kinase. FEBS Lett. 471, 151-155 (Pubitemid 30190055)
41. Meggio, F., Donella Deana, A., Ruzzene, M., Brunati, A. M., Cesaro, L., Guerra, B., Meyer, T., Mett, H., Fabbro, D., Furet, P., et al. (1995) Different susceptibility of protein kinases to staurosporine inhibition. Kinetic studies and molecular bases for the resistance of protein kinase CK2. Eur. J. Biochem. 234, 317-322
42. Fields, G. B., and Noble, R. L. (1990) Solid phase peptide synthesis utilizing 9-fluorenylmethoxycarbonyl amino acids. Int. J. Pept. Protein Res. 35, 161-214 (Pubitemid 20126875)