Phosphorylation decreases ubiquitylation of the thiazide-sensitive cotransporter NCC and subsequent clathrin-mediated endocytosis

Journal of Biological Chemistry

Volumn 289, Issue 19, 2014, Pages 13347-13361

  Rosenbaek, Lena L ^a   Kortenoeven, Marleen L A ^a   Aroankins, Takwa S ^a   Fenton, Robert A ^a  

^a AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL MEMBRANES; DIMERS; MOLECULAR BIOLOGY; SODIUM CHLORIDE;

APICAL PLASMA MEMBRANE; GLYCOSYLATED; IMMUNOGOLD ELECTRON MICROSCOPIES; MADIN-DARBY CANINE KIDNEYS; SPECIFIC INHIBITORS; TRANSPORT ACTIVITY; TRANSPORT PROTEINS; UBIQUITYLATION;

PHOSPHORYLATION;

ASPARTIC ACID; BETA CYCLODEXTRIN; CLATHRIN; FILIPIN; NYSTATIN; SERINE; SODIUM CHLORIDE; SODIUM CHLORIDE COTRANSPORTER; TETRACYCLINE; THREONINE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOCYTOSIS; INTERNALIZATION; KIDNEY DISTAL TUBULE; MDCK CELL LINE; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SODIUM TRANSPORT; UBIQUITINATION;

ENDOCYTOSIS; EPITHELIUM; PHOSPHORYLATION; PLASMA MEMBRANE; TRAFFICKING; UBIQUITYLATION;

ANIMALS; CLATHRIN; DOGS; ENDOCYTOSIS; HUMANS; ION TRANSPORT; MADIN DARBY CANINE KIDNEY CELLS; PHOSPHORYLATION; RATS; SODIUM CHLORIDE; SOLUTE CARRIER FAMILY 12, MEMBER 3; UBIQUITINATION;

EID: 84900386364     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.543710     Document Type: Article

References (54)

1. Gamba, G. (2005) Molecular physiology and pathophysiology of electroneutral cation-chloride cotransporters. Physiol. Rev. 85, 423-493
2. Plotkin, M. D., Kaplan, M. R., Verlander, J. W., Lee, W. S., Brown, D., Poch, E., Gullans, S. R., and Hebert, S. C. (1996) Localization of the thiazide sensitive Na-Cl cotransporter, rTSC1 in the rat kidney. Kidney Int. 50, 174-183
3. Gamba, G., Miyanoshita, A., Lombardi, M., Lytton, J., Lee, W. S., Hediger, M. A., and Hebert, S. C. (1994) Molecular cloning, primary structure, and characterization of two members of the mammalian electroneutral sodium-(potassium) -chloride cotransporter family expressed in kidney. J. Biol. Chem. 269, 17713-17722
4. De Jong, J. C., Willems, P. H., Mooren, F. J., Van Den Heuvel, L. P., Knoers, N. V., and Bindels, R. J. (2003) The structural unit of the thiazide-sensitive NaCl cotransporter is a homodimer. J. Biol. Chem. 278, 24302-24307
5. Hoover, R. S., Poch, E., Monroy, A., Vázquez, N., Nishio, T., Gamba, G., and Hebert, S. C. (2003) N-Glycosylation at two sites critically alters thiazide binding and activity of the rat thiazide-sensitive Na (+):Cl (-) cotransporter. J. Am. Soc. Nephrol. 14, 271-282
6. Simon, D. B., Nelson-Williams, C., Bia, M. J., Ellison, D., Karet, F. E., Molina, A. M., Vaara, I., Iwata, F., Cushner, H. M., Koolen, M., Gainza, F. J., Gitleman, H. J., and Lifton, R. P. (1996) Gitelman's variant of Bartter's syndrome, inherited hypokalaemic alkalosis, is caused by mutations in the thiazide-sensitive Na-Cl cotransporter. Nat. Genet. 12, 24-30
7. Mastroianni, N., Bettinelli, A., Bianchetti, M., Colussi, G., De Fusco, M., Sereni, F., Ballabio, A., and Casari, G. (1996) Novel molecular variants of the Na-Cl cotransporter gene are responsible for Gitelman syndrome. Am. J. Hum. Genet. 59, 1019-1026
8. Lemmink, H. H., Knoers, N. V., Károlyi, L., Van Dijk, H., Niaudet, P., Antignac, C., Guay-Woodford, L. M., Goodyer, P. R., Carel, J. C., Hermes, A., Seyberth, H. W., Monnens, L. A., and Van Den Heuvel, L. P. (1998) Novel mutations in the thiazide-sensitive NaCl cotransporter gene in patients with Gitelman syndrome with predominant localization to the Cterminal domain. Kidney Int. 54, 720-730
9. Monkawa, T., Kurihara, I., Kobayashi, K., Hayashi, M., and Saruta, T. (2000) Novel mutations in thiazide-sensitive Na-Cl cotransporter gene of patients with Gitelman's syndrome. J. Am. Soc. Nephrol. 11, 65-70
10. Subramanya, A. R., Liu, J., Ellison, D. H., Wade, J. B., and Welling, P. A. (2009) WNK4 diverts the thiazide-sensitive NaCl cotransporter to the lysosome and stimulates AP-3 interaction. J. Biol. Chem. 284, 18471-18480
11. Cai, H., Cebotaru, V., Wang, Y. H., Zhang, X. M., Cebotaru, L., Guggino, S. E., and Guggino, W. B. (2006) WNK4 kinase regulates surface expression of the human sodium chloride cotransporter in mammalian cells. Kidney Int. 69, 2162-2170
12. Ko, B., Joshi, L. M., Cooke, L. L., Vazquez, N., Musch, M. W., Hebert, S. C., Gamba, G., and Hoover, R. S. (2007) Phorbol ester stimulation of RasGRP1 regulates the sodium-chloride cotransporter by a PKC-independent pathway. Proc. Natl. Acad. Sci. U. S. A. 104, 20120-20125
13. Ko, B., Kamsteeg, E. J., Cooke, L. L., Moddes, L. N., Deen, P. M., and Hoover, R. S. (2010) RasGRP1 stimulation enhances ubiquitination and endocytosis of the sodium-chloride cotransporter. Am. J. Physiol. Renal Physiol. 299, F300-F309
14. Lu, H., Sun, T. X., Bouley, R., Blackburn, K., McLaughlin, M., and Brown, D. (2004) Inhibition of endocytosis causes phosphorylation (S256) -independent plasma membrane accumulation of AQP2. Am. J. Physiol. Renal Physiol. 286, F233-F243
15. Ares, G. R., and Ortiz, P. A. (2012) Dynamin2, clathrin, and lipid rafts mediate endocytosis of the apical Na/K/2Cl cotransporter NKCC2 in thick ascending limbs. J. Biol. Chem. 287, 37824-37834
16. +-Cl cotransporter by the WNK-regulated kinases SPAK and OSR1. J. Cell Sci. 121, 675-684
17. +:Cl cotransporter is activated and phosphorylated at the amino-terminal domain upon intracellular chloride depletion. J. Biol. Chem. 281, 28755-28763
18. Pedersen, N. B., Hofmeister, M. V., Rosenbaek, L. L., Nielsen, J., and Fenton, R. A. (2010) Vasopressin induces phosphorylation of the thiazidesensitive sodium chloride cotransporter in the distal convoluted tubule. Kidney Int. 78, 160-169
19. McCormick, J. A., Mutig, K., Nelson, J. H., Saritas, T., Hoorn, E. J., Yang, C. L., Rogers, S., Curry, J., Delpire, E., Bachmann, S., and Ellison, D. H. (2011) A SPAK isoform switch modulates renal salt transport and blood pressure. Cell Metab. 14, 352-364
20. Shi, H., Asher, C., Chigaev, A., Yung, Y., Reuveny, E., Seger, R., and Garty, H. (2002) Interactions ofα andβ ENaC with Nedd4 can be facilitated by an ERK-mediated phosphorylation. J. Biol. Chem. 277, 13539-13547
21. Shi, H., Asher, C., Yung, Y., Kligman, L., Reuveny, E., Seger, R., and Garty, H. (2002) Casein kinase 2 specifically binds to and phosphorylates the carboxy termini of ENaC subunits. Eur. J. Biochem. 269, 4551-4558
22. Moeller, H. B., Praetorius, J., Rützler, M. R., and Fenton, R. A. (2010) Phosphorylation of aquaporin-2 regulates its endocytosis and proteinprotein interactions. Proc. Natl. Acad. Sci. U. S. A. 107, 424-429
23. Rice, W. L., Zhang, Y., Chen, Y., Matsuzaki, T., Brown, D., and Lu, H. A. (2012) Differential, phosphorylation-dependent trafficking of AQP2 in LLC-PK1 cells. PLoS One 7, e32843
24. Kim, G. H., Masilamani, S., Turner, R., Mitchell, C., Wade, J. B., and Knepper, M. A. (1998) The thiazide-sensitive Na-Cl cotransporter is an aldosteroneinduced protein. Proc. Natl. Acad. Sci. U. S. A. 95, 14552-14557
25. Fenton, R. A., Brønd, L., Nielsen, S., and Praetorius, J. (2007) Cellular and subcellular distribution of the type-2 vasopressin receptor in the kidney. Am. J. Physiol. Renal Physiol. 293, F748-F760
26. Rosenbaek, L. L., Assentoft, M., Pedersen, N. B., MacAulay, N., and Fenton, R. A. (2012) Characterization of a novel phosphorylation site in the sodium-chloride cotransporter, NCC. J. Physiol. 590, 6121-6139
27. Fröhlich, O., Klein, J. D., Smith, P. M., Sands, J. M., and Gunn, R. B. (2004) Urea transport in MDCK cells that are stably transfected with UT-A1. Am. J. Physiol. Cell Physiol. 286, C1264-C1270
28. Dutta, D., Williamson, C. D., Cole, N. B., and Donaldson, J. G. (2012) Pitstop 2 is a potent inhibitor of clathrin-independent endocytosis. PLoS One 7, e45799
29. Hossain Khan, M. Z., Sohara, E., Ohta, A., Chiga, M., Inoue, Y., Isobe, K., Wakabayashi, M., Oi, K., Rai, T., Sasaki, S., and Uchida, S. (2012) Phosphorylation of Na-Cl cotransporter by OSR1 and SPAK kinases regulates its ubiquitination. Biochem. Biophys. Res. Commun. 425, 456-461
30. Mutig, K., Saritas, T., Uchida, S., Kahl, T., Borowski, T., Paliege, A., Böhlick, A., Bleich, M., Shan, Q., and Bachmann, S. (2010) Short-term stimulation of the thiazide-sensitive Naα-Cl cotransporter by vasopressin involves phosphorylation and membrane translocation. Am. J. Physiol. Renal Physiol. 298, F502-F509
31. Sandberg, M. B., Riquier, A. D., Pihakaski-Maunsbach, K., McDonough, A. A., and Maunsbach, A. B. (2007) ANG II provokes acute trafficking of distal tubule Naα-Cl cotransporter to apical membrane. Am. J. Physiol. Renal Physiol. 293, F662-F669
32. - cotransporter (NCC) in response to a high-salt diet. Am. J. Physiol. Renal Physiol. 291, F503-F508
33. Ko, B., Mistry, A. C., Hanson, L., Mallick, R., Cooke, L. L., Hack, B. K., Cunningham, P., and Hoover, R. S. (2012) A new model of the distal convoluted tubule. Am. J. Physiol. Renal Physiol. 303, F700-F710
34. Gesek, F. A., and Friedman, P. A. (1992) Mechanism of calcium transport stimulated by chlorothiazide in mouse distal convoluted tubule cells. J. Clin. Invest. 90, 429-438
35. Peng, K. C., Cluzeaud, F., Bens, M., Duong Van Huyen, J. P., Wioland, M. A., Lacave, R., and Vandewalle, A. (1999) Tissue and cell distribution of the multidrug resistance-Associated protein (MRP) in mouse intestine and kidney. J. Histochem. Cytochem. 47, 757-768
36. Markadieu, N., San-Cristobal, P., Nair, A. V., Verkaart, S., Lenssen, E., Tudpor, K., Van Zeeland, F., Loffing, J., Bindels, R. J., and Hoenderop, J. G. (2012) A primary culture of distal convoluted tubules expressing functional thiazide-sensitive NaCl transport. Am. J. Physiol. Renal Physiol. 303, F886-F892
37. Yang, S. S., Yamauchi, K., Rai, T., Hiyama, A., Sohara, E., Suzuki, T., Itoh, T., Suda, S., Sasaki, S., and Uchida, S. (2005) Regulation of apical localization of the thiazide-sensitive NaCl cotransporter by WNK4 in polarized epithelial cells. Biochem. Biophys. Res. Commun. 330, 410-414
38. Zhou, B., Zhuang, J., Gu, D., Wang, H., Cebotaru, L., Guggino, W. B., and Cai, H. (2010) WNK4 enhances the degradation of NCC through a sortilinmediated lysosomal pathway. J. Am. Soc. Nephrol. 21, 82-92
39. De Jong, J. C., Van Der Vliet, W. A., Van Den Heuvel, L. P., Willems, P. H., Knoers, N. V., and Bindels, R. J. (2002) Functional expression of mutations in the human NaCl cotransporter: evidence for impaired routing mechanisms in Gitelman's syndrome. J. Am. Soc. Nephrol. 13, 1442-1448
40. Kunchaparty, S., Palcso, M., Berkman, J., Velázquez, H., Desir, G. V., Bernstein, P., Reilly, R. F., and Ellison, D. H. (1999) Defective processing and expression of thiazide-sensitive Na-Cl cotransporter as a cause of Gitelman's syndrome. Am. J. Physiol. 277, F643-F649
41. Ares, G. R., and Ortiz, P. A. (2010) Constitutive endocytosis and recycling of NKCC2 in rat thick ascending limbs. Am. J. Physiol. Renal Physiol. 299, F1193-F1202
42. Fang, L., Garuti, R., Kim, B. Y., Wade, J. B., and Welling, P. A. (2009) The ARH adaptor protein regulates endocytosis of the ROMK potassium secretory channel in mouse kidney. J. Clin. Invest. 119, 3278-3289
43. Mayor, S., and Pagano, R. E. (2007) Pathways of clathrin-independent endocytosis. Nat. Rev. Mol. Cell Biol. 8, 603-612
44. Traub, L. M. (2009) Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat. Rev. Mol. Cell Biol. 10, 583-596
45. Fujimoto, T. (1993) Calcium pump of the plasma membrane is localized in caveolae. J. Cell Biol. 120, 1147-1157
46. Shimkets, R. A., Lifton, R. P., and Canessa, C. M. (1997) The activity of the epithelial sodium channel is regulated by clathrin-mediated endocytosis. J. Biol. Chem. 272, 25537-25541
47. Sun, T. X., Van Hoek, A., Huang, Y., Bouley, R., McLaughlin, M., and Brown, D. (2002) Aquaporin-2 localization in clathrin-coated pits: inhibition of endocytosis by dominant-negative dynamin. Am. J. Physiol. Renal Physiol. 282, F998-F1011
48. + exchanger, NHE3, is internalized through a clathrin-mediated pathway. J. Biol. Chem. 274, 37551-37558
49. Huang, H., Feng, X., Zhuang, J., Fröhlich, O., Klein, J. D., Cai, H., Sands, J. M., and Chen, G. (2010) Internalization of UT-A1 urea transporter is dynamin dependent and mediated by both caveolae- and clathrin-coated pit pathways. Am. J. Physiol. Renal Physiol. 299, F1389-F1395
50. Chiga, M., Rai, T., Yang, S. S., Ohta, A., Takizawa, T., Sasaki, S., and Uchida, S. (2008) Dietary salt regulates the phosphorylation of OSR1/SPAK kinases and the sodium chloride cotransporter through aldosterone. Kidney Int. 74, 1403-1409
51. - cotransporter NCC in vivo is regulated by dietary salt, potassium, and SGK1. Am. J. Physiol. Renal Physiol. 297, F704-F712
52. Wagner, S. A., Beli, P., Weinert, B. T., Schölz, C., Kelstrup, C. D., Young, C., Nielsen, M. L., Olsen, J. V., Brakebusch, C., and Choudhary, C. (2012) Proteomic analyses reveal divergent ubiquitylation site patterns in murine tissues. Mol. Cell. Proteomics 11, 1578-1585
53. +-Cl cotransporter is regulated by protein phosphatase PP4. Can. J. Physiol. Pharmacol. 88, 986-995
54. Sorensen, M. V., Grossmann, S., Roesinger, M., Gresko, N., Todkar, A. P., Barmettler, G., Ziegler, U., Odermatt, A., Loffing-Cueni, D., and Loffing, J. (2013) Rapid dephosphorylation of the renal sodium chloride cotransporter in response to oral potassium intake in mice. Kidney Int. 83, 811-824