FoxO1 inhibits transcription and membrane trafficking of epithelial Na+ channel

Journal of Cell Science

Volumn 128, Issue 19, 2015, Pages 3621-3630

  Shen, Yachen ^a   Xu, Weifeng ^a   You, Hui ^a   Su, Dongming ^a   Xing, Jing ^a   Li, Min ^a   Li, Lei ^a   Liang, Xiubin ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

Author keywords

14 3 3 ; Epithelial Na+ channel; FoxO1; Protein phosphorylation; Protein protein interaction

Indexed keywords

EPITHELIAL SODIUM CHANNEL; INSULIN; MESSENGER RNA; TRANSCRIPTION FACTOR FKHR; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, MOUSE;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; CELL MIGRATION; HUMAN; HUMAN CELL; INSULIN TREATMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; ANIMAL; GENETICS; IMMUNOPRECIPITATION; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; EPITHELIAL SODIUM CHANNELS; FORKHEAD TRANSCRIPTION FACTORS; IMMUNOPRECIPITATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84946038007     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.171876     Document Type: Article

References (42)

1. Aitken, A., Baxter, H., Dubois, T., Clokie, S., Mackie, S., Mitchell, K., Peden, A. and Zemlickova, E. (2002). Specificity of 14-3-3 isoform dimer interactions and phosphorylation. Biochem. Soc. Trans. 30, 351-360.
2. Altomonte, J., Cong, L., Harbaran, S., Richter, A., Xu, J., Meseck, M. and Dong, H. H. (2004). Foxo1 mediates insulin action on apoC-III and triglyceride metabolism. J. Clin. Invest. 114, 1493-1503.
3. Arriola, D. J., Mayo, S. L., Skarra, D. V., Benson, C. A. and Thackray, V. G. (2012). FOXO1 transcription factor inhibits luteinizing hormone beta gene expression in pituitary gonadotrope cells. J. Biol. Chem. 287, 33424-33435.
4. Ayala, J. E., Streeper, R. S., Desgrosellier, J. S., Durham, S. K., Suwanichkul, A., Svitek, C. A., Goldman, J. K., Barr, F. G., Powell, D. R. and O'Brien, R. M. (1999). Conservation of an insulin response unit between mouse and human glucose-6-phosphatase catalytic subunit gene promoters: transcription factor FKHR binds the insulin response sequence. Diabetes 48, 1885-1889.
5. Barthel, A., Schmoll, D. and Unterman, T. G. (2005). FoxO proteins in insulin action and metabolism. Trends Endocrinol. Metab. 16, 183-189.
6. Bhalla, V., Daidié, D., Li, H., Pao, A. C., LaGrange, L. P., Wang, J., Vandewalle, A., Stockand, J. D., Staub, O. and Pearce, D. (2005). Serum-and glucocorticoidregulated kinase 1 regulates ubiquitin ligase neural precursor cell-expressed, developmentally down-regulated protein 4-2 by inducing interaction with 14-3-3. Mol. Endocrinol. 19, 3073-3084.
7. Bhalla, V., Soundararajan, R., Pao, A. C., Li, H. and Pearce, D. (2006). Disinhibitory pathways for control of sodium transport: regulation of ENaC by SGK1 and GILZ. Am. J. Physiol. Renal Physiol. 291, F714-F721.
8. Blazer-Yost, B. L., Liu, X. and Helman, S. I. (1998). Hormonal regulation of ENaCs: insulin and aldosterone. Am. J. Physiol. 274, C1373-C1379.
9. Blazer-Yost, B. L., Esterman, M. A. and Vlahos, C. J. (2003). Insulin-stimulated trafficking of ENaC in renal cells requires PI 3-kinase activity. Am. J. Physiol. Cell Physiol. 284, C1645-C1653.
10. Brownawell, A. M., Kops, G. J., Macara, I. G. and Burgering, B. M. T. (2001). Inhibition of nuclear import by protein kinase B (Akt) regulates the subcellular distribution and activity of the forkhead transcription factor AFX. Mol. Cell. Biol. 21, 3534-3546.
11. Brunet, A., Park, J., Tran, H., Hu, L. S., Hemmings, B. A. and Greenberg, M. E. (2001). Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol. Cell. Biol. 21, 952-965.
12. Bubien, J. K. (2010). Epithelial Na+ channel (ENaC), hormones, and hypertension. J. Biol. Chem. 285, 23527-23531.
13. Butterworth, M. B. (2010). Regulation of the epithelial sodium channel (ENaC) by membrane trafficking. Biochim. Biophys. Acta 1802, 1166-1177.
14. Butterworth, M. B., Edinger, R. S., Frizzell, R. A. and Johnson, J. P. (2009). Regulation of the epithelial sodium channel by membrane trafficking. Am. J. Physiol. Renal Physiol. 296, F10-F24.
15. Cai, B., Wang, N., Mao, W., You, T., Lu, Y., Li, X., Ye, B., Li, F. and Xu, H. (2014). Deletion of FoxO1 leads to shortening of QRS by increasing Na+ channel activity through enhanced expression of both cardiac NaV1.5 and beta3 subunit. J. Mol. Cell. Cardiol. 74, 297-306.
16. Chaudhri, M., Scarabel, M. and Aitken, A. (2003). Mammalian and yeast 14-3-3 isoforms form distinct patterns of dimers in vivo. Biochem. Biophys. Res. Commun. 300, 679-685.
17. Ergonul, Z., Frindt, G. and Palmer, L. G. (2006). Regulation of maturation and processing of ENaC subunits in the rat kidney. Am. J. Physiol. Renal Physiol. 291, F683-F693.
18. Frindt, G., Masilamani, S., Knepper, M. A. and Palmer, L. G. (2001). Activation of epithelial Na channels during short-term Na deprivation. Am. J. Physiol. Renal Physiol. 280, F112-F118.
19. Furuyama, T., Nakazawa, T., Nakano, I. and Mori, N. (2000). Identification of the differential distribution patterns of mRNAs and consensus binding sequences for mouse DAF-16 homologues. Biochem. J. 349, 629-634.
20. Hu, M. C.-T., Lee, D.-F., Xia, W., Golfman, L. S., Ou-Yang, F., Yang, J.-Y., Zou, Y., Bao, S., Hanada, N., Saso, H. et al. (2004). IkappaB kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell 117, 225-237.
21. Huang, H., Regan, K. M., Lou, Z., Chen, J. and Tindall, D. J. (2006). CDK2-dependent phosphorylation of FOXO1 as an apoptotic response to DNA damage. Science 314, 294-297.
22. Ilatovskaya, D. V., Levchenko, V., Brands, M. W., Pavlov, T. S. and Staruschenko, A. (2015). Cross-talk between insulin and IGF-1 receptors in the cortical collecting duct principal cells: implication for ENaC-mediated Na+ reabsorption. Am. J. Physiol. Renal Physiol. 308, F713-F719.
23. Kamagate, A. and Dong, H. H. (2008). FoxO1 integrates insulin signaling to VLDL production. Cell Cycle 7, 3162-3170.
24. Kamagate, A., Qu, S., Perdomo, G., Su, D., Kim, D. H., Slusher, S., Meseck, M. and Dong, H. H. (2008). FoxO1 mediates insulin-dependent regulation of hepatic VLDL production in mice. J. Clin. Invest. 118, 2347-2364.
25. Liang, X., Peters, K. W., Butterworth, M. B. and Frizzell, R. A. (2006). 14-3-3 isoforms are induced by aldosterone and participate in its regulation of epithelial sodium channels. J. Biol. Chem. 281, 16323-16332.
26. Liang, X., Butterworth, M. B., Peters, K. W., Walker, W. H. and Frizzell, R. A. (2008). An obligatory heterodimer of 14-3-3beta and 14-3-3epsilon is required for aldosterone regulation of the epithelial sodium channel. J. Biol. Chem. 283, 27418-27425.
27. Liang, X., Butterworth, M. B., Peters, K. W. and Frizzell, R. A. (2010). AS160 modulates aldosterone-stimulated epithelial sodium channel forward trafficking. Mol. Biol. Cell 21, 2024-2033.
28. Loffing, J., Zecevic, M., Feraille, E., Kaissling, B., Asher, C., Rossier, B. C., Firestone, G. L., Pearce, D. and Verrey, F. (2001). Aldosterone induces rapid apical translocation of ENaC in early portion of renal collecting system: possible role of SGK. Am. J. Physiol. Renal Physiol. 280, F675-F682.
29. Malik, B., Price, S. R., Mitch, W. E., Yue, Q. and Eaton, D. C. (2006). Regulation of epithelial sodium channels by the ubiquitin-proteasome proteolytic pathway. Am. J. Physiol. Renal Physiol. 290, F1285-F1294.
30. Mao, W., You, T., Ye, B., Li, X., Dong, H. H., Hill, J. A., Li, F. and Xu, H. (2012). Reactive oxygen species suppress cardiac NaV1.5 expression through Foxo1. PLoS ONE 7, e32738.
31. Masilamani, S., Kim, G.-H., Mitchell, C., Wade, J. B. and Knepper, M. A. (1999). Aldosterone-mediated regulation of ENaC alpha, beta, and gamma subunit proteins in rat kidney. J. Clin. Invest. 104, R19-R23.
32. Philip-Couderc, P., Tavares, N. I., Roatti, A., Lerch, R., Montessuit, C. and Baertschi, A. J. (2008). Forkhead transcription factors coordinate expression of myocardial KATP channel subunits and energy metabolism. Circ. Res. 102, e20-e35.
33. Pratt, J. H. (2005). Central role for ENaC in development of hypertension. J. Am. Soc. Nephrol. 16, 3154-3159.
34. Puigserver, P., Rhee, J., Donovan, J., Walkey, C. J., Yoon, J. C., Oriente, F., Kitamura, Y., Altomonte, J., Dong, H., Accili, D. et al. (2003). Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1alpha interaction. Nature 423, 550-555.
35. Rena, G., Prescott, A. R., Guo, S., Cohen, P. and Unterman, T. G. (2001). Roles of the forkhead in rhabdomyosarcoma (FKHR) phosphorylation sites in regulating 14-3-3 binding, transactivation and nuclear targetting. Biochem. J. 354, 605-612.
36. Robert-Nicoud, M., Flahaut, M., Elalouf, J.-M., Nicod, M., Salinas, M., Bens, M., Doucet, A., Wincker, P., Artiguenave, F., Horisberger, J.-D. et al. (2001). Transcriptome of a mouse kidney cortical collecting duct cell line: effects of aldosterone and vasopressin. Proc. Natl. Acad. Sci. USA 98, 2712-2716.
37. Soundararajan, R., Melters, D., Shih, I.-C., Wang, J. and Pearce, D. (2009). Epithelial sodium channel regulated by differential composition of a signaling complex. Proc. Natl. Acad. Sci. USA 106, 7804-7809.
38. Soundararajan, R., Pearce, D., Hughey, R. P. and Kleyman, T. R. (2010a). Role of epithelial sodium channels and their regulators in hypertension. J. Biol. Chem. 285, 30363-30369.
39. Soundararajan, R., Wang, J., Melters, D. and Pearce, D. (2010b). Glucocorticoidinduced Leucine zipper 1 stimulates the epithelial sodium channel by regulating serum-and glucocorticoid-induced kinase 1 stability and subcellular localization. J. Biol. Chem. 285, 39905-39913.
40. Stahl, M., Dijkers, P. F., Kops, G. J. P. L., Lens, S. M. A., Coffer, P. J., Burgering, B. M. T. and Medema, R. H. (2002). The forkhead transcription factor FoxO regulates transcription of p27Kip1 and Bim in response to IL-2. J. Immunol. 168, 5024-5031.
41. Wilker, E. and Yaffe, M. B. (2004). 14-3-3 Proteins-a focus on cancer and human disease. J. Mol. Cell. Cardiol. 37, 633-642.
42. Yaffe, M. B. (2002). How do 14-3-3 proteins work?-Gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett. 513, 53-57.