Resveratrol Inhibits the Epithelial Sodium Channel via Phopshoinositides and AMP-Activated Protein Kinase in Kidney Collecting Duct Cells

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Weixel, Kelly M ^b   Marciszyn, Allison ^a   Alzamora, Rodrigo ^a   Li, Hui ^a   Fischer, Oliver ^a   Edinger, Robert S ^a   Hallows, Kenneth R ^a   Johnson, John P ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b WASHINGTON AND JEFFERSON COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITHELIAL SODIUM CHANNEL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; RESVERATROL;

ANIMAL CELL; ARTICLE; CELL POLARITY; CONTROLLED STUDY; DRUG ACTIVITY; DRUG INHIBITION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE SILENCING; GENETIC TRANSFECTION; KIDNEY COLLECTING TUBULE; MICROSCOPY; MOUSE; NONHUMAN; PROTEIN DEPLETION; PROTEIN FUNCTION; RENAL PROTECTION; SODIUM TRANSPORT;

AMILORIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELL LINE; CELLS, CULTURED; EPITHELIAL SODIUM CHANNELS; IMMUNOBLOTTING; KIDNEY TUBULES, COLLECTING; MICE; PHOSPHATIDYLINOSITOLS; RNA, SMALL INTERFERING; STILBENES;

EID: 84886261673     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078019     Document Type: Article

References (40)

1. Butterworth MB, Edinger RS, Frizzell RA, Johnson JP, (2009) Regulation of the epithelial sodium channel by membrane trafficking. Am J Physiol Renal Physiol 296: F10-24.
2. Bhalla V, Hallows KR, (2008) Mechanisms of ENaC regulation and clinical implications. JAmSocNephrol 19: 1845-1854.
3. Shimkets RA, Warnock DG, Bositis CM, Nelson-Williams C, Hansson JH, et al. (1994) Liddle's syndrome: heritable human hypertension caused by mutations in the beta subunit of the epithelial sodium channel. Cell 79: 407-414.
4. Hansson JH, Nelson-Williams C, Suzuki H, Schild L, Shimkets R, et al. (1995) Hypertension caused by a truncated epithelial sodium channel gamma subunit: genetic heterogeneity of Liddle syndrome. NatGenet 11: 76-82.
5. Chang SS, Grunder S, Hanukoglu A, Rosler A, Mathew PM, et al. (1996) Mutations in subunits of the epithelial sodium channel cause salt wasting with hyperkalemic acidosis, pseudoaldosteronism type 1. Nature Genetics 13: 248-250.
6. Wang H, Traub LM, Weixel KM, Hawryluk MJ, Shah N, et al. (2006) Clathrin-mediated endocytosis of the epithelial sodium channel. Role of epsin. J BiolChem 281: 14129-14135.
7. Weixel KM, Edinger RS, Kester L, Guerriero CJ, Wang H, et al. (2007) Phosphatidylinositol 4-phosphate 5-kinase reduces cell surface expression of the epithelial sodium channel (ENaC) in cultured collecting duct cells. J BiolChem 282: 36534-36542.
8. Record RD, Froelich L, Vlahos CJ, Blazer-Yost BL, (1998) Phosphatidylinositol 3-kinase activation is required for insulin-stimulated sodium transport in A6 cells. American Journal of Physiology 274: E611-E617.
9. Blazer-Yost BL, Paunescu TG, Helman SI, Lee KD, Vlahos CJ, (1999) Phosphoinositide 3-kinase is required for aldosterone-regulated sodium reabsorption. American Journal of Physiology 277: C531-C536.
10. Gonzalez-Rodriguez E, Gaeggeler HP, Rossier BC, (2007) IGF-1 vs insulin: respective roles in modulating sodium transport via the PI-3 kinase/Sgk1 pathway in a cortical collecting duct cell line. Kidney Int 71: 116-125.
11. Pochynyuk O, Tong Q, Medina J, Vandewalle A, Staruschenko A, et al. (2007) Molecular determinants of PI(4,5)P2 and PI(3,4,5)P3 regulation of the epithelial Na+ channel. J Gen Physiol 130: 399-413.
12. Staruschenko A, Pochynyuk O, Vandewalle A, Bugaj V, Stockand JD, (2007) Acute regulation of the epithelial Na+ channel by phosphatidylinositide 3-OH kinase signaling in native collecting duct principal cells. J Am Soc Nephrol 18: 1652-1661.
13. Pochynyuk O, Tong Q, Staruschenko A, Stockand JD, (2007) Binding and direct activation of the epithelial Na+ channel (ENaC) by phosphatidylinositides. J Physiol 580: 365-372.
14. Pochynyuk O, Tong Q, Staruschenko A, Ma HP, Stockand JD, (2006) Regulation of the epithelial Na+ channel (ENaC) by phosphatidylinositides. Am J Physiol Renal Physiol 290: F949-957.
15. Pervaiz S, Holme AL, (2009) Resveratrol: its biologic targets and functional activity. Antioxid Redox Signal 11: 2851-2897.
16. Chung JH, Manganiello V, Dyck JR, (2012) Resveratrol as a calorie restriction mimetic: therapeutic implications. Trends Cell Biol 22: 546-554.
17. Xu Q, Si LY, (2012) Resveratrol role in cardiovascular and metabolic health and potential mechanisms of action. Nutr Res 32: 648-658.
18. Baur JA, Sinclair DA, (2006) Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 5: 493-506.
19. Dolinsky VW, Chakrabarti S, Pereira TJ, Oka T, Levasseur J, et al. (2013) Resveratrol prevents hypertension and cardiac hypertrophy in hypertensive rats and mice. Biochim Biophys Acta.
20. Rimbaud S, Ruiz M, Piquereau J, Mateo P, Fortin D, et al. (2011) Resveratrol improves survival, hemodynamics and energetics in a rat model of hypertension leading to heart failure. PLoS One 6: e26391.
21. Das S, Fraga CG, Das DK, (2006) Cardioprotective effect of resveratrol via HO-1 expression involves p38 map kinase and PI-3-kinase signaling, but does not involve NFkappaB. Free Radic Res 40: 1066-1075.
22. Ding DF, You N, Wu XM, Xu JR, Hu AP, et al. (2010) Resveratrol attenuates renal hypertrophy in early-stage diabetes by activating AMPK. Am J Nephrol 31: 363-374.
23. Park CE, Kim MJ, Lee JH, Min BI, Bae H, et al. (2007) Resveratrol stimulates glucose transport in C2C12 myotubes by activating AMP-activated protein kinase. Exp Mol Med 39: 222-229.
24. Park SJ, Ahmad F, Philp A, Baar K, Williams T, et al. (2012) Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases. Cell 148: 421-433.
25. Bhalla V, Oyster NM, Fitch AC, Wijngaarden MA, Neumann D, et al. (2006) AMP-activated kinase inhibits the epithelial Na+ channel through functional regulation of the ubiquitin ligase Nedd4-2. J BiolChem 281: 26159-26169.
26. Bens M, Vallet V, Cluzeaud F, Pascual-Letallec L, Kahn A, et al. (1999) Corticosteroid-dependent sodium transport in a novel immortalized mouse collecting duct principal cell line. JAmSocNephrol 10: 923-934.
27. Alzamora R, Gong F, Rondanino C, Lee JK, Smolak C, et al. (2010) AMP-activated protein kinase inhibits KCNQ1 channels through regulation of the ubiquitin ligase Nedd4-2 in renal epithelial cells. Am J Physiol Renal Physiol 299: F1308-1319.
28. Ooms LM, Dyson JM, Kong AM, Mitchell CA, (2009) Analysis of phosphatidylinositol 3,4,5 trisphosphate 5-phosphatase activity by in vitro and in vivo assays. Methods Mol Biol 462: 223-239.
29. Frojdo S, Cozzone D, Vidal H, Pirola L, (2007) Resveratrol is a class IA phosphoinositide 3-kinase inhibitor. Biochem J 406: 511-518.
30. Wang J, Knight ZA, Fiedler D, Williams O, Shokat KM, et al. (2008) Activity of the p110-alpha subunit of phosphatidylinositol-3-kinase is required for activation of epithelial sodium transport. Am J Physiol Renal Physiol 295: F843-850.
31. Carattino MD, Edinger RS, Grieser HJ, Wise R, Neumann D, et al. (2005) Epithelial sodium channel inhibition by AMP-activated protein kinase in oocytes and polarized renal epithelial cells. J BiolChem 280: 17608-17616.
32. Liu M, Wilk SA, Wang A, Zhou L, Wang RH, et al. (2010) Resveratrol inhibits mTOR signaling by promoting the interaction between mTOR and DEPTOR. J Biol Chem 285: 36387-36394.
33. Kitada M, Kume S, Imaizumi N, Koya D, (2011) Resveratrol improves oxidative stress and protects against diabetic nephropathy through normalization of Mn-SOD dysfunction in AMPK/SIRT1-independent pathway. Diabetes 60: 634-643.
34. Chen KH, Hung CC, Hsu HH, Jing YH, Yang CW, et al. (2011) Resveratrol ameliorates early diabetic nephropathy associated with suppression of augmented TGF-beta/smad and ERK1/2 signaling in streptozotocin-induced diabetic rats. Chem Biol Interact 190: 45-53.
35. Faber AC, Dufort FJ, Blair D, Wagner D, Roberts MF, et al. (2006) Inhibition of phosphatidylinositol 3-kinase-mediated glucose metabolism coincides with resveratrol-induced cell cycle arrest in human diffuse large B-cell lymphomas. Biochem Pharmacol 72: 1246-1256.
36. Sexton E, Van Themsche C, LeBlanc K, Parent S, Lemoine P, et al. (2006) Resveratrol interferes with AKT activity and triggers apoptosis in human uterine cancer cells. Mol Cancer 5: 45.
37. Jang M, Cai L, Udeani GO, Slowing KV, Thomas CF, et al. (1997) Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275: 218-220.
38. Pochynyuk O, Bugaj V, Stockand JD, (2008) Physiologic regulation of the epithelial sodium channel by phosphatidylinositides. Curr Opin Nephrol Hypertens 17: 533-540.
39. Hallows KR, Mount PF, Pastor-Soler NM, Power DA, (2010) Role of the energy sensor AMP-activated protein kinase in renal physiology and disease. Am J Physiol Renal Physiol 298: F1067-1077.
40. Staruschenko A, Patel P, Tong Q, Medina JL, Stockand JD, (2004) Ras activates the epithelial Na(+) channel through phosphoinositide 3-OH kinase signaling. J Biol Chem 279: 37771-37778.