Regulation of (Pro)renin receptor expression in mIMCD via the GSK-3β-NFAT5-SIRT-1 signaling pathway

American Journal of Physiology - Renal Physiology

Volumn 307, Issue 5, 2014, Pages

  Quadri, Syed ^a   Siragy, Helmy M ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

(Pro)renin receptor; Inner medullary collecting duct; NFAT5; SIRT 1

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; MESSENGER RNA; PRORENIN RECEPTOR; SIRTUIN 1; SMALL INTERFERING RNA; SODIUM CHLORIDE; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFAT5; UNCLASSIFIED DRUG; 6-CHLORO-2,3,4,9-TETRAHYDRO-1H-CARBAZOLE-1-CARBOXAMIDE; CARBAZOLE DERIVATIVE; CELL SURFACE RECEPTOR; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; NFAT5 PROTEIN, MOUSE; RELA PROTEIN, MOUSE; SIRT1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ARTICLE; ENZYME PHOSPHORYLATION; KIDNEY COLLECTING TUBULE; MOUSE; NEPHRON; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SODIUM RESTRICTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; IN VITRO STUDY; PHOSPHORYLATION; PHYSIOLOGY;

ANIMALS; CARBAZOLES; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; GLYCOGEN SYNTHASE KINASE 3; IN VITRO TECHNIQUES; KIDNEY TUBULES, COLLECTING; MICE; PHOSPHORYLATION; RECEPTORS, CELL SURFACE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SIRTUIN 1; SODIUM CHLORIDE; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTORS;

EID: 84906896013     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00245.2014     Document Type: Article

References (48)

1. Advani A, Kelly DJ, Cox AJ, White KE, Advani SL, Thai K, Connelly KA, Yuen D, Trogadis J, Herzenberg AM, Kuliszewski MA, Leong-Poi H, Gilbert RE. The (Pro)renin receptor: site-specific and functional linkage to the vacuolar H-ATPase in the kidney. Hypertension 54: 261-269, 2009.
2. Anastasiou D, Krek W. SIRT1: linking adaptive cellular responses to aging-associated changes in organismal physiology. Physiology (Bethesda) 21: 404-410, 2006.
3. Batenburg WW, Krop M, Garrelds IM, de Vries R, de Bruin RJ, Burckle CA, Muller DN, Bader M, Nguyen G, Danser AH. Prorenin is the endogenous agonist of the (pro)renin receptor. Binding kinetics of renin and prorenin in rat vascular smooth muscle cells overexpressing the human (pro)renin receptor. J Hypertens 25: 2441-2453, 2007.
4. Boudreau RL, Davidson BL. Generation of hairpin-based RNAi vectors for biological and therapeutic application. Methods Enzymol 507: 275-296, 2012.
5. Cai Q, Ferraris JD, Burg MB. High NaCl increases TonEBP/OREBP mRNA and protein by stabilizing its mRNA. Am J Physiol Renal Physiol 289: F803-F807, 2005.
6. Chen SW, Chen YX, Zhang XR, Qian H, Chen WZ, Xie WF. Targeted inhibition of platelet-derived growth factor receptor-beta subunit in hepatic stellate cells ameliorates hepatic fibrosis in rats. Gene Ther 15: 1424-1435, 2008.
7. Dahl SC, Handler JS, Kwon HM. Hypertonicity-induced phosphorylation and nuclear localization of the transcription factor TonEBP. Am J Physiol Cell Physiol 280: C248-C253, 2001.
8. Ferraris JD, Williams CK, Persaud P, Zhang Z, Chen Y, Burg MB. Activity of the TonEBP/OREBP transactivation domain varies directly with extracellular NaCl concentration. Proc Natl Acad Sci USA 99: 739-744, 2002.
9. Ferri N, Greco CM, Maiocchi G, Corsini A. Aliskiren reduces prorenin receptor expression and activity in cultured human aortic smooth muscle cells. J Renin Angiotensin Aldosterone Syst 12: 469-474, 2011.
10. Frindt G, Masilamani S, Knepper MA, Palmer LG. Activation of epithelial Na channels during short-term Na deprivation. Am J Physiol Renal Physiol 280: F112-F118, 2001.
11. Gonzalez AA, Lara LS, Luffman C, Seth DM, Prieto MC. Soluble form of the (pro)renin receptor is augmented in the collecting duct and urine of chronic angiotensin II-dependent hypertensive rats. Hypertension 57: 859-864, 2011.
12. Guarente L. Sir2 links chromatin silencing, metabolism, and aging. Genes Dev 14: 1021-1026, 2000.
13. Hall JE, Brands MW, Henegar JR. Angiotensin II and long-term arterial pressure regulation: the overriding dominance of the kidney. J Am Soc Nephrol 10(Suppl 12): S258-S265, 1999.
14. Halterman JA, Kwon HM, Wamhoff BR. Tonicity-independent regulation of the osmosensitive transcription factor TonEBP (NFAT5). Am J Physiol Cell Physiol 302: C1-C8, 2012.
15. Hao S, Zhao H, Darzynkiewicz Z, Battula S, Ferreri NR. Differential regulation of NFAT5 by NKCC2 isoforms in medullary thick ascending limb (mTAL) cells. Am J Physiol Renal Physiol 300: F966-F975, 2011.
16. Hasegawa K, Wakino S, Simic P, Sakamaki Y, Minakuchi H, Fujimura K, Hosoya K, Komatsu M, Kaneko Y, Kanda T, Kubota E, Tokuyama H, Hayashi K, Guarente L, Itoh H. Renal tubular Sirt1 attenuates diabetic albuminuria by epigenetically suppressing claudin-1 overexpression in podocytes. Nat Med 19: 1496-1504, 2013.
17. Ho SN. The role of NFAT5/TonEBP in establishing an optimal intracellular environment. Arch Biochem Biophys 413: 151-157, 2003.
18. Huang J, Matavelli LC, Siragy HM. Renal (pro)renin receptor contributes to development of diabetic kidney disease through transforming growth factor-beta1-connective tissue growth factor signalling cascade. Clin Exp Pharmacol Physiol 38: 215-221, 2011.
19. Huang J, Siragy HM. Regulation of (pro)renin receptor expression by glucose-induced mitogen-activated protein kinase, nuclear factor-kappaB, and activator protein-1 signaling pathways. Endocrinology 151: 3317-3325, 2010.
20. Huang J, Siragy HM. Sodium depletion enhances renal expression of (pro)renin receptor via cyclic GMP-protein kinase G signaling pathway. Hypertension 59: 317-323, 2012.
21. Huang W, Liu H, Wang T, Zhang T, Kuang J, Luo Y, Chung SS, Yuan L, Yang JY. Tonicity-responsive microRNAs contribute to the maximal induction of osmoregulatory transcription factor OREBP in response to high-NaCl hypertonicity. Nucleic Acids Res 39: 475-485, 2011.
22. Hughes K, Pulverer BJ, Theocharous P, Woodgett JR. Baculovirus-mediated expression and characterisation of rat glycogen synthase kinase-3 beta, the mammalian homologue of the Drosophila melanogaster zeste-white 3sgg homeotic gene product. Eur J Biochem 203: 305-311, 1992.
23. Hur EM, Zhou FQ. GSK3 signalling in neural development. Nat Rev Neurosci 11: 539-551, 2010.
24. Irarrazabal CE, Burg MB, Ward SG, Ferraris JD. Phosphatidylinositol 3-kinase mediates activation of ATM by high NaCl and by ionizing radiation: Role in osmoprotective transcriptional regulation. Proc Natl Acad Sci USA 103: 8882-8887, 2006.
25. Kauppinen A, Suuronen T, Ojala J, Kaarniranta K, Salminen A. Antagonistic crosstalk between NF-kappaB and SIRT1 in the regulation of inflammation and metabolic disorders. Cell Signal 25: 1939-1948, 2013.
26. Ko BC, Turck CW, Lee KW, Yang Y, Chung SS. Purification, identification, and characterization of an osmotic response element binding protein. Biochem Biophys Res Commun 270: 52-61, 2000.
27. Lawrence T. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol 1: a001651, 2009.
28. Li XC, Zhuo JL. Phosphoproteomic analysis of AT1 receptor-mediated signaling responses in proximal tubules of angiotensin II-induced hypertensive rats. Kidney Int 80: 620-632, 2011.
29. Liu TF, Yoza BK, El Gazzar M, Vachharajani VT, McCall CE. NAD-dependent SIRT1 deacetylase participates in epigenetic reprogramming during endotoxin tolerance. J Biol Chem 286: 9856-9864, 2011.
30. Matavelli LC, Huang J, Siragy HM. In vivo regulation of renal expression of (pro)renin receptor by a low-sodium diet. Am J Physiol Renal Physiol 303: F1652-F1657, 2012.
31. Matavelli LC, Huang J, Siragy HM. (Pro)renin receptor contributes to diabetic nephropathy by enhancing renal inflammation. Clin Exp Pharmacol Physiol 37: 277-282, 2010.
32. Miyakawa H, Woo SK, Dahl SC, Handler JS, Kwon HM. Tonicity-responsive enhancer binding protein, a rel-like protein that stimulates transcription in response to hypertonicity. Proc Natl Acad Sci USA 96: 2538-2542, 1999.
33. Miyazaki R, Ichiki T, Hashimoto T, Inanaga K, Imayama I, Sadoshima J, Sunagawa K. SIRT1, a longevity gene, downregulates angiotensin II type 1 receptor expression in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 28: 1263-1269, 2008.
34. Navar LG, Prieto MC, Satou R, Kobori H. Intrarenal angiotensin II and its contribution to the genesis of chronic hypertension. Curr Opin Pharmacol 11: 180-186, 2011.
35. Nguyen G, Delarue F, Burckle C, Bouzhir L, Giller T, Sraer JD. Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin. J Clin Invest 109: 1417-1427, 2002.
36. Nguyen G, Muller DN. The biology of the (pro)renin receptor. J Am Soc Nephrol 21: 18-23, 2010.
37. Prieto MC, Botros FT, Kavanagh K, Navar LG. Prorenin receptor in distal nephron segments of 2-kidney, 1-clip Goldblatt hypertensive rats. Ochsner J 13: 26-32, 2013.
38. Salminen A, Kauppinen A, Suuronen T, Kaarniranta K. SIRT1 longevity factor suppresses NF-kappaB-driven immune responses: regulation of aging via NF-kappaB acetylation? Bioessays 30: 939-942, 2008.
39. Thomson DM, Hancock CR, Evanson BG, Kenney SG, Malan BB, Mongillo AD, Brown JD, Hepworth S, Fillmore N, Parcell AC, Kooyman DL, Winder WW. Skeletal muscle dysfunction in muscle-specific LKB1 knockout mice. J Appl Physiol 108: 1775-1785, 2010.
40. Wang F, Lu X, Peng K, Zhou L, Li C, Wang W, Yu X, Kohan DE, Zhou SF, Yang T. COX-2 mediates angiotensin II-induced (pro)renin receptor expression in the rat renal medulla. Am J Physiol Renal Physiol 307: F25-F32, 2014.
41. Wang H, Brown J, Martin M. Glycogen synthase kinase 3: a point of convergence for the host inflammatory response. Cytokine 53: 130-140, 2011.
42. Yan W, Fang Z, Yang Q, Dong H, Lu Y, Lei C, Xiong L. SirT1 mediates hyperbaric oxygen preconditioning-induced ischemic tolerance in rat brain. J Cereb Blood Flow Metab 33: 396-406, 2013.
43. Yang H, Zhang W, Pan H, Feldser HG, Lainez E, Miller C, Leung S, Zhong Z, Zhao H, Sweitzer S, Considine T, Riera T, Suri V, White B, Ellis JL, Vlasuk GP, Loh C. SIRT1 activators suppress inflammatory responses through promotion of p65 deacetylation and inhibition of NF-kappaB activity. PLoS One 7: e46364, 2012.
44. Yang T, Park JM, Arend L, Huang Y, Topaloglu R, Pasumarthy A, Praetorius H, Spring K, Briggs JP, Schnermann J. Low chloride stimulation of prostaglandin E2 release and cyclooxygenase-2 expression in a mouse macula densa cell line. J Biol Chem 275: 37922-37929, 2000.
45. Yao H, Rahman I. Perspectives on translational and therapeutic aspects of SIRT1 in inflammaging and senescence. Biochem Pharmacol 84: 1332-1339, 2012.
46. Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, Frye RA, Mayo MW. Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J 23: 2369-2380, 2004.
47. Ying W. NAD /NADH and NADP /NADPH in cellular functions and cell death: regulation and biological consequences. Antioxid Redox Signal 10: 179-206, 2008.
48. Zhou X, Wang H, Burg MB, Ferraris JD. Inhibitory phosphorylation of GSK-3 by AKT, PKA, and PI3K contributes to high NaCl-induced activation of the transcription factor NFAT5 (TonEBP/OREBP). Am J Physiol Renal Physiol 304: F908-F917, 2013.