Enhanced glycogen synthase kinase-3β activity mediates podocyte apoptosis under diabetic conditions

Apoptosis

Volumn 19, Issue 12, 2014, Pages 1678-1690

  Paeng, Jisun ^a   Chang, Jae Hyun ^b   Lee, Sun Ha ^a   Nam, Bo Young ^a   Kang, Hye Young ^a   Kim, Seonghun ^a   Oh, Hyung Jung ^a   Park, Jung Tak ^a   Han, Seung Hyeok ^a   Yoo, Tae Hyun ^a   Kang, Shin Wook ^a  

^a Yonsei University College of Medicine   (South Korea)

^b Gachon University College of Medicine   (South Korea)

Author keywords

Apoptosis; Diabetic nephropathy; GSK 3 ; Podocyte

Indexed keywords

ALBUMIN; BETA CATENIN; CASPASE 3; GAMMA INTERFERON; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; STREPTOZOCIN; TYROSINE; 6-BROMOINDIRUBIN-3'-OXIME; APOPTOSIS REGULATORY PROTEIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; INDOLE DERIVATIVE; OXIME;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL LOSS; CONTROLLED STUDY; DIABETIC NEPHROPATHY; ENZYME ACTIVITY; GLOMERULUS; GLUCOSE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; TUNEL ASSAY; URINE LEVEL; WESTERN BLOTTING; ALBUMINURIA; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ALBUMINURIA; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; DIABETES MELLITUS, EXPERIMENTAL; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3; INDOLES; KIDNEY GLOMERULUS; MALE; OXIMES; PHOSPHORYLATION; PODOCYTES; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; STREPTOZOCIN; TYROSINE;

EID: 84941766470     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-014-1037-5     Document Type: Article

References (54)

1. Frame S, Cohen P (2001) GSK3 takes centre stage more than 20 years after its discovery. Biochem J 359:1-16
2. Woodgett JR (1990) Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J 9:2431-2438
3. Doble BW, Woodgett JR (2003) GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 116:1175-1186
4. Ferkey DM, Kimelman D (2000) GSK-3: new thoughts on an old enzyme. Dev Biol 225:471-479
5. Sinha D, Wang Z, Ruchalski KL, Levine JS, Krishnan S, Lieberthal W, Schwartz JH, Borkan SC (2005) Lithium activates the Wnt and phosphatidylinositol 3-kinase Akt signaling pathways to promote cell survival in the absence of soluble survival factors. Am J Physiol Renal Physiol 288:F703-F713
6. Pap M, Cooper GM (2002) Role of translation initiation factor 2B in control of cell survival by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3beta signaling pathway. Mol Cell Biol 22:578-586
7. Sanchez JF, Sniderhan LF, Williamson AL, Fan S, Chakraborty-Sett S, Maggirwar SB (2003) Glycogen synthase kinase 3beta-mediated apoptosis of primary cortical astrocytes involves inhibition of nuclear factor kappaB signaling. Mol Cell Biol 23:4649-4662
8. Jacobs KM, Bhave SR, Ferraro DJ, Jaboin JJ, Hallahan DE, Thotala D (2012) GSK-3beta: a bifunctional role in cell death pathways. Int J Cell Biol 2012:930710
9. Gong R, Rifai A, Ge Y, Chen S, Dworkin LD (2008) Hepatocyte growth factor suppresses proinflammatory NFkappaB activation through GSK3beta inactivation in renal tubular epithelial cells. J Biol Chem 283:7401-7410
10. Gong R, Rifai A, Dworkin LD (2005) Activation of PI3 K-Akt-GSK3beta pathway mediates hepatocyte growth factor inhibition of RANTES expression in renal tubular epithelial cells. Biochem Biophys Res Commun 330:27-33
11. Nelson PJ, Cantley L (2010) GSK3beta plays dirty in acute kidney injury. J Am Soc Nephrol 21:199-200
12. Ge Y, Si J, Tian L, Zhuang S, Dworkin LD, Gong R (2011) Conditional ablation of glycogen synthase kinase 3beta in postnatal mouse kidney. Lab Invest 91:85-96
13. Wang Z, Havasi A, Gall J, Bonegio R, Li Z, Mao H, Schwartz JH, Borkan SC (2010) GSK3beta promotes apoptosis after renal ischemic injury. J Am Soc Nephrol 21:284-294
14. Lin CL, Wang JY, Huang YT, Kuo YH, Surendran K, Wang FS (2006) Wnt/beta-catenin signaling modulates survival of high glucose-stressed mesangial cells. J Am Soc Nephrol 17:2812-2820
15. Boini KM, Amann K, Kempe D, Alessi DR, Lang F (2009) Proteinuria in mice expressing PKB/SGK-resistant GSK3. Am J Physiol Renal Physiol 296:F153-F159
16. George B, Vollenbroker B, Saleem MA, Huber TB, Pavenstadt H, Weide T (2011) GSK3beta inactivation in podocytes results in decreased phosphorylation of p70S6 K accompanied by cytoskeletal rearrangements and inhibited motility. Am J Physiol Renal Physiol 300:F1152-F1162
17. Shankland SJ (2006) The podocyte's response to injury: role in proteinuria and glomerulosclerosis. Kidney Int 69:2131-2147
18. Wolf G, Chen S, Ziyadeh FN (2005) From the periphery of the glomerular capillary wall toward the center of disease: podocyte injury comes of age in diabetic nephropathy. Diabetes 54:1626-1634
19. Li JJ, Kwak SJ, Jung DS, Kim JJ, Yoo TH, Ryu DR et al (2007) Podocyte biology in diabetic nephropathy. Kidney Int 72:S36-S42
20. Susztak K, Raff AC, Schiffer M, Bottinger EP (2006) Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes 55:225-233
21. Steffes MW, Schmidt D, McCrery R, Basgen JM (2001) Glomerular cell number in normal subjects and in type 1 diabetic patients. Kidney Int 59:2104-2113
22. Verzola D, Gandolfo MT, Ferrario F, Rastaldi MP, Villaggio B, Gianiorio F et al (2007) Apoptosis in the kidneys of patients with type II diabetic nephropathy. Kidney Int 72:1262-1272
23. Mundel P, Reiser J, Zuniga Mejia Borja A, Pavenstadt H, Davidson GR, Kriz W, Zeller R (1997) Rearrangements of the cytoskeleton and cell contacts induce process formation during differentiation of conditionally immortalized mouse podocyte cell lines. Exp Cell Res 236:248-258
24. Kang SW, Adler SG, Nast CC, LaPage J, Gu JL, Nadler JL, Natarajan R (2001) 12-lipoxygenase is increased in glucose-stimulated mesangial cells and in experimental diabetic nephropathy. Kidney Int 59:1354-1362
25. Doublier S, Ruotsalainen V, Salvidio G, Lupia E, Biancone L, Conaldi PG, Reponen P, Tryggvason K, Camussi G (2001) Nephrin redistribution on podocytes is a potential mechanism for proteinuria in patients with primary acquired nephrotic syndrome. Am J Pathol 158:1723-1731
26. Sanden SK, Wiggins JE, Goyal M, Riggs LK, Wiggins RC (2003) Evaluation of a thick and thin section method for estimation of podocyte number, glomerular volume, and glomerular volume per podocyte in rat kidney with Wilms' tumor-1 protein used as a podocyte nuclear marker. J Am Soc Nephrol 14:2484-2493
27. Beurel E, Jope RS (2006) The paradoxical pro- and anti-apoptotic actions of GSK3 in the intrinsic and extrinsic apoptosis signaling pathways. Prog Neurobiol 79:173-189
28. Linseman DA, Butts BD, Precht TA, Phelps RA, Le SS, Laessig TA, Bouchard RJ, Florez-McClure ML, Heidenreich KA (2004) Glycogen synthase kinase-3beta phosphorylates Bax and promotes its mitochondrial localization during neuronal apoptosis. J Neurosci 24:9993-10002
29. Maurer U, Charvet C, Wagman AS, Dejardin E, Green DR (2006) Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol Cell 21:749-760
30. Zhao Y, Altman BJ, Coloff JL, Herman CE, Jacobs SR, Wieman HL et al (2007) Glycogen synthase kinase 3alpha and 3beta mediate a glucose-sensitive antiapoptotic signaling pathway to stabilize Mcl-1. Mol Cell Biol 27:4328-4339
31. Obligado SH, Ibraghimov-Beskrovnaya O, Zuk A, Meijer L, Nelson PJ (2008) CDK/GSK-3 inhibitors as therapeutic agents for parenchymal renal diseases. Kidney Int 73:684-690
32. Hongisto V, Smeds N, Brecht S, Herdegen T, Courtney MJ, Coffey ET (2003) Lithium blocks the c-Jun stress response and protects neurons via its action on glycogen synthase kinase 3. Mol Cell Biol 23:6027-6036
33. Tan J, Zhuang L, Leong HS, Iyer NG, Liu ET, Yu Q (2005) Pharmacologic modulation of glycogen synthase kinase-3beta promotes p53-dependent apoptosis through a direct Bax-mediated mitochondrial pathway in colorectal cancer cells. Cancer Res 65:9012-9020
34. Watcharasit P, Bijur GN, Song L, Zhu J, Chen X, Jope RS (2003) Glycogen synthase kinase-3beta (GSK3beta) binds to and promotes the actions of p53. J Biol Chem 278:48872-48879
35. Liao X, Zhang L, Thrasher JB, Du J, Li B (2003) Glycogen synthase kinase-3beta suppression eliminates tumor necrosis factor-related apoptosis-inducing ligand resistance in prostate cancer. Mol Cancer Ther 2:1215-1222
36. Song L, Zhou T, Jope RS (2004) Lithium facilitates apoptotic signaling induced by activation of the Fas death domain-containing receptor. BMC Neurosci 5:20
37. Lan Y, Liu X, Zhang R, Wang K, Wang Y, Hua ZC (2013) Lithium enhances TRAIL-induced apoptosis in human lung carcinoma A549 cells. Biometals 26:241-254
38. Kotliarova S, Pastorino S, Kovell LC, Kotliarov Y, Song H, Zhang W et al (2008) Glycogen synthase kinase-3 inhibition induces glioma cell death through c-MYC, nuclear factor-kappaB, and glucose regulation. Cancer Res 68:6643-6651
39. Pagtalunan ME, Miller PL, Jumping-Eagle S, Nelson RG, Myers BD, Rennke HG, Coplon NS, Sun L, Meyer TW (1997) Podocyte loss and progressive glomerular injury in type II diabetes. J Clin Invest 99:342-348
40. Tejada T, Catanuto P, Ijaz A, Santos JV, Xia X, Sanchez P, Sanabria N, Lenz O, Elliot SJ, Fornoni A (2008) Failure to phosphorylate AKT in podocytes from mice with early diabetic nephropathy promotes cell death. Kidney Int 73:1385-1393
41. Shin SY, Kim CG, Jho EH, Rho MS, Kim YS, Kim YH, Lee YH (2004) Hydrogen peroxide negatively modulates Wnt signaling through downregulation of beta-catenin. Cancer Lett 212:225-231
42. King TD, Jope RS (2005) Inhibition of glycogen synthase kinase-3 protects cells from intrinsic but not extrinsic oxidative stress. NeuroReport 16:597-601
43. Song L, De Sarno P, Jope RS (2002) Central role of glycogen synthase kinase-3beta in endoplasmic reticulum stress-induced caspase-3 activation. J Biol Chem 277:44701-44708
44. Kim AJ, Shi Y, Austin RC, Werstuck GH (2005) Valproate protects cells from ER stress-induced lipid accumulation and apoptosis by inhibiting glycogen synthase kinase-3. J Cell Sci 118:89-99
45. Lorz C, Benito-Martin A, Boucherot A, Ucero AC, Rastaldi MP, Henger A et al (2008) The death ligand TRAIL in diabetic nephropathy. J Am Soc Nephrol 19:904-914
46. Huang H, He X (2008) Wnt/beta-catenin signaling: new (and old) players and new insights. Curr Opin Cell Biol 20:119-125
47. Kaga S, Zhan L, Altaf E, Maulik N (2006) Glycogen synthase kinase-3beta/beta-catenin promotes angiogenic and anti-apoptotic signaling through the induction of VEGF, Bcl-2 and survivin expression in rat ischemic preconditioned myocardium. J Mol Cell Cardiol 40:138-147
48. Rao R, Hao CM, Breyer MD (2004) Hypertonic stress activates glycogen synthase kinase 3beta-mediated apoptosis of renal medullary interstitial cells, suppressing an NFkappaB-driven cyclooxygenase-2-dependent survival pathway. J Biol Chem 279:3949-3955
49. Dai C, Stolz DB, Kiss LP, Monga SP, Holzman LB, Liu Y (2009) Wnt/beta-catenin signaling promotes podocyte dysfunction and albuminuria. J Am Soc Nephrol 20:1997-2008
50. Li Z, Xu J, Xu P, Liu S, Yang Z (2013) Wnt/beta-catenin signalling pathway mediates high glucose induced cell injury through activation of TRPC6 in podocytes. Cell Prolif 46:76-85
51. Kato H, Gruenwald A, Suh JH, Miner JH, Barisoni-Thomas L, Taketo MM, Faul C, Millar SE, Holzman LB, Susztak K (2011) Wnt/beta-catenin pathway in podocytes integrates cell adhesion, differentiation, and survival. J Biol Chem 286:26003-26015
52. Kanzariya NR, Patel RK, Patel NJ (2011) Antidiabetic and vasoprotective activity of lithium: role of glycogen synthase kinase-3. Indian J Pharmacol 43:433-436
53. Kwon TH, Laursen UH, Marples D, Maunsbach AB, Knepper MA, Frokiaer J, Nielsen S (2000) Altered expression of renal AQPs and Na(+) transporters in rats with lithium-induced NDI. Am J Physiol Renal Physiol 279:F552-F564
54. Meijer L, Skaltsounis AL, Magiatis P, Polychronopoulos P, Knockaert M, Leost M et al (2003) GSK-3-selective inhibitors derived from Tyrian purple indirubins. Chem Biol 10:1255-1266