Casein kinase 2 binds to the C terminus of Na+/H+ exchanger 3 (NHE3) and stimulates NHE3 basal activity by phosphorylating a separate site in NHE3

Molecular Biology of the Cell

Volumn 19, Issue 9, 2008, Pages 3859-3870

  Sarker, Rafiquel ^a   Grønborg, Mads ^a,c   Cha, Boyoung ^a   Mohan, Sachin ^a   Chen, Yueping ^a   Pandey, Akhilesh ^a   Litchfield, David ^b   Donowitz, Mark ^a   Li, Xuhang ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WESTERN UNIVERSITY   (Canada)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; SODIUM PROTON EXCHANGE PROTEIN 3;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DOWN REGULATION; ENDOCYTOSIS; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; WESTERN BLOTTING;

ANIMALS; BENZIMIDAZOLES; CACO-2 CELLS; CASEIN KINASE II; CELL MEMBRANE; CHROMATOGRAPHY, LIQUID; ENDOCYTOSIS; FIBROBLASTS; HUMANS; MASS SPECTROMETRY; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SODIUM; SODIUM-HYDROGEN ANTIPORTER;

EID: 55549139194     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-01-0019     Document Type: Article

References (45)

1. Akhter, S., Cavet, M. E., Tse, C. M., and Donowitz, M. (2000). C-Terminal domain of Na+/H+ exchanger isoform 3 are involved in the basal and serum-stimulated membrane trafficking of the exchanger. Biochemistry 39, 1990-2000.
2. Allen, D., Fakler, B., Maylie, J., and Adelman, J. P. (2007). Organization and regulation of small conductance Ca2+-activated K+ channel multiprotein complexes. J. Neurosci. 27, 2369-2376.
3. Arrigoni, G., Marin, O., Pagano, M. A., Settimo, L., Paolin, B., Meggio, F., and Pinna, L. A. (2004). Phosphorylation of calmodulin fragments by protein kinase CK2. Mechanistic aspects and structural consequences. Biochemistry 43, 12788-12798.
4. Bildl, W. et al. (2004). Protein kinase CK2 is coassembled with small conductance Ca(2+)-activated K+ channels and regulates channel gating. Neuron 43, 847-858.
5. Bolanos-Garcia, V. M., Fernandez-Recio, J., Allende, J. E., and Blundell, T. L. (2006). Identifying interaction motifs in CK2beta-a ubiquitous kinase regulatory subunit. Trends Biochem. Sci. 31, 654-661.
6. Bone, D. B., Robillard, K. R., Stolk, M., and Hammond, J. R. (2007). Differential regulation of mouse equilibrative nucleoside transporter 1 (mENT1) splice variants by protein kinase CK2. Mol. Membr. Biol. 24, 294-303.
7. Cai, Y. et al. (2004). Calcium dependence of polycystin-2 channel activity is modulated by phosphorylation at Ser812. J. Biol. Chem. 279, 19987-19995.
8. Cha, B., Tse, M., Yun, C., Kovbasnjuk, O., Mohan, S., Hubbard, A., Arpin, M., and Donowitz, M. (2006). The NHE3 juxtamembrane cytoplasmic domain directly binds ezrin: dual role in NHE3 trafficking and mobility in the brush border. Mol. Biol. Cell 17, 2661-2673.
9. Donowitz, M., and Li, X. (2007). Regulatory binding partners and complexes of NHE3. Physiol. Rev. 87, 825-872.
10. Donowitz, M., and Welsh, M. J. (1986). Ca2+ and cAMP in regulation of intestinal Na, K and Cl transport. Annu. Rev. Physiol. 48, 135-150.
11. Donowitz, M., Wicks, J., Madara, J. L., and Sharp, G. W. (1985). Studies on role of calmodulin in Ca2+ regulation of rabbit ileal Na and Cl transport. Am. J. Physiol. 248, G726-G740.
12. Faust, M., and Montenarh, M. (2000). Subcellular localization of protein kinase CK2. A key to its function? Cell Tissue Res. 301, 329-340.
13. Filhol, O., Martiel, J. L., and Cochet, C. (2004). Protein kinase CK 2, a new view of an old molecular complex. EMBO Rep. 5, 351-355.
14. Glavy, J. S., Horwitz, S. B., and Orr, G. A. (1997). Identification of the in vivo phosphorylation sites for acidic-directed kinases in murine mdr1b P-glycoprotein. J. Biol. Chem. 272, 5909-5914.
15. Gronborg, M., Bunkenborg, J., Kristiansen, T. Z., Jensen, O. N., Yeo, C. J., Hruban, R. H., Maitra, A., Goggins, M. G., and Pandey, A. (2004). Comprehensive proteomic analysis of human pancreatic juice. J. Proteome Res. 3, 1042-1055.
16. Janecki, A. J., Montrose, M. H., Zimniak, P., Zweibaum, A., Tse, C. M., Khurana, S., and Donowitz, M. (1998). Subcellular redistribution is involved in acute regulation of the brush border Na+/H+ exchanger isoform 3 in human colon adenocarcinoma cell line Caco-2. Protein kinase C-mediated inhibition of the exchanger. J. Biol. Chem. 273, 8790-8798.
17. Jones, S., and Yakel, J. L. (2003). Casein kinase ii (protein kinase ck2) regulates serotonin 5-ht(3) receptor channel function in ng108-15 cells. Neuroscience 119, 629-634.
18. Krantz, D. E., Peter, D., Liu, Y., and Edwards, R. H. (1997). Phosphorylation of a vesicular monoamine transporter by casein kinase II. J. Biol. Chem. 272, 6752-6759.
19. Lamprecht, G., Heil, A., Baisch, S., Lin-Wu, E., Yun, C. C., Kalbacher, H., Gregor, M., and Seidler, U. (2002). The down regulated in adenoma (dra) gene product binds to the second PDZ domain of the NHE3 kinase a regulatory protein (E3KARP), potentially linking intestinal Cl-/HCO3-exchange to Na+/H+ exchange. Biochemistry 41, 12336-12342.
20. Levine, S. A., Montrose, M. H., Tse, C. M., and Donowitz, M. (1993). Kinetics and regulation of three cloned mammalian Na+/H+ exchangers stably expressed in a fibroblast cell line. J. Biol. Chem. 268, 25527-25535.
21. Levine, S. A., Nath, S. K., Yun, C. H., Yip, J. W., Montrose, M., Donowitz, M., and Tse, C. M. (1995). Separate C-terminal domains of the epithelial specific brush border Na+/H+ exchanger isoform NHE3 are involved in stimulation and inhibition by protein kinases/growth factors. J. Biol. Chem. 270, 13716-13725.
22. Lieberman, D. N. and Mody, I. (1999). Casein kinase-II regulates NMDA channel function in hippocampal neurons. Nat. Neurosci. 2, 125-132.
23. Litchfield, D. W. (2003). Protein kinase CK 2, structure, regulation and role in cellular decisions of life and death. Biochem. J. 369, 1-15.
24. Macica, C. M., and Kaczmarek, L. K. (2001). Casein kinase 2 determines the voltage dependence of the Kv3.1 channel in auditory neurons and transfected cells. J. Neurosci. 21, 1160-1168.
25. Madrid, R., Le Maout, S., Barrault, M. B., Janvier, K., Benichou, S., and Merot, J. (2001). Polarized trafficking and surface expression of the AQP4 water channel are coordinated by serial and regulated interactions with different clathrin-adaptor complexes. EMBO J. 20, 7008-7021.
26. Meggio, F., and Pinna, L. A. (2005). One-thousand-and-one substrates of protein kinase CK2? FASEB J. 17, 349-368.
27. Moe, O. W. (1999). Acute regulation of proximal tubule apical membrane Na/H exchanger NHE-3, role of phosphorylation, protein trafficking, and regulatory factors. J. Am. Soc. Nephrol. 10, 2412-2425.
28. Murtazina, R., Kovbasnjuk, O., Donowitz, M., and Li, X. (2006). Na+/H+ exchanger NHE3 activity and trafficking are lipid Raft-dependent. J. Biol. Chem. 281, 17845-17855.
29. Obenauer, J. C., Cantley, L. C., and Yaffe, M. B. (2003). Scansite 2.0, Proteomie-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31, 3635-3641.
30. Olsten, M. E., and Litchfield, D. W. (2004). Order or chaos? An evaluation of the regulation of protein kinase CK2. Biochem. Cell Biol. 82, 681-693.
31. Olsten, M. E., Weber, J. E., and Litchfield, D. W. (2005). CK2 interacting proteins: emerging paradigms for CK2 regulation. Mol. Cell Biochem. 274, 115-124.
32. Pagano, M. A., Meggio, F., Ruzzene, M., Andrzejewska, M., Kazimierczuk, Z., and Pinna, L. A. (2004). 2-Dimethylamino-4,5,6,7-tetrabromo-1H- benzimidazole: a novel powerful and selective inhibitor of protein kinase CK2. Biochem. Biophys. Res. Commun. 321, 1040-1044.
33. Pessin, J. E., Thurmond, D. C., Elmendorf, J. S., Coker, K. J., and Okada, S. (1999). Molecular basis of insulin-stimulated GLUT4 vesicle trafficking. Location! Location! Location! J. Biol. Chem. 274, 2593-2596.
34. Roosbeek, S. et al. (2004). Phosphorylation by protein kinase CK2 modulates the activity of the ATP binding cassette A1 transporter. J. Biol. Chem. 279, 37779-37788.
35. Ruzzene, M., Penzo, D., and Pinna, L. A. (2002). Protein kinase CK2 inhibitor 4, 5, 6, 7-tetrabromobenzotriazole (TBB) induces apoptosis and caspase-dependent degradation of haematopoietic linage cell-specific protein 1 (HS1) in Jurkat cells. Biochem. J. 364, 41-47.
36. Sarno, S., Moro, S., Meggio, F., Zagotto, G. L., Dal Ben, D., Ghisellini, P., Battistutta, R., Zanoti, G., and Pinna, L. A. (2002). Toward the rational design of protein kinase casein kinase-2 inhibitors. Pharmacol. Ther. 93, 159-168.
37. Sarno, S., Ruzzene, M., Frascella, P., Pagano, M. A., Meggio, F., Zambon, A., Mazzorana, M., Di Maira, G., Lucchini, V., and Pinna, L. A. (2005). Development and exploitation of CK2 inhibitors. Mol. Cell Biochem. 274, 69-76.
38. 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.
39. Theis-Febvre, N., Martel, V., Laudet, B., Souchier, C., Grunwald, D., Cochet, C., and Filhol, O. (2005). Highlighting protein kinase CK2 movement in living cells. Mol. Cell. Biochem. 274, 15-22.
40. Treharne, K. J. et al. (2007). Protein kinase CK2, cystic fibrosis transmembrane conductance regulator, and the deltaF508 mutation: F508 deletion disrupts a kinase-binding site. J. Biol. Chem. 282, 10804-10813.
41. Wang, D., Sun, H., Lang, F., and Yun, C. C. (2005). Activation of NHE3 by dexamethasone requires phosphorylation of NHE3 at Ser663 by SGK1. Am. J. Physiol. Cell Physiol. 289, C802-C810.
42. Watson, R. T., and Pessin, J. E. (2001). Intracellular organization of insulin signaling and GLUT4 translocation. Recent Prog. Horm. Res. 56, 175-193.
43. Wiederkehr, M. R., Zhao, H., and Moe, O. W. (1999). Acute regulation of Na/H exchanger NHE3 activity by protein kinase C: role of NHE3 phosphorylation. Am. J. Physiol. 276, C1205-C1217.
44. Yip, K. P., Tse, C. M., McDonough, A. A., and Marsh, D. J. (1998). Redistribution of Na+/H+ exchanger isoform NHE3 in proximal tubules induced by acute and chronic hypertension. Am. J. Physiol. 275, F565-F575.
45. Zachos, N. C., Tse, M., and Donowitz, M. (2005). Molecular physiology of intestinal Na+/H+ exchange. Annu. Rev. Physiol. 67, 411-443.