Activation of general control nonderepressible 2 kinase protects human glomerular endothelial cells from harmful high-glucose-induced molecular pathways

International Urology and Nephrology

Volumn 48, Issue 10, 2016, Pages 1731-1739

  Eleftheriadis, Theodoros ^a   Tsogka, Konstantina ^a   Pissas, Georgios ^a   Antoniadi, Georgia ^a   Liakopoulos, Vassilios ^a   Stefanidis, Ioannis ^a  

^a UNIVERSITY OF THESSALY   (Greece)

Author keywords

AGEs; Aldose reductase; Diabetic nephropathy; Endothelium; GCN2 kinase; Hexosamine; PKC; ROS

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ENZYME ACTIVATOR; GENERAL CONTROL NONDEREPRESSIBLE 2 KINASE; GLUCOSE; GLUCOSE TRANSPORTER 1; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEXOSAMINE; METHYLGLYOXAL; N ACETYLGLUCOSAMINE; PHOSPHOTRANSFERASE; POLYOL; PROTEIN DERIVATIVE; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; SORBITOL; TRYPTOPHANOL; UNCLASSIFIED DRUG; GLUCOSE BLOOD LEVEL; GLYCERALDEHYDE 3-PHOSPHATE DEHYDROGENASE (304-313); PEPTIDE FRAGMENT; TRYPTOPHAN;

ARTICLE; COLORIMETRY; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GLOMERULAR ENDOTHELIAL CELL; GLOMERULUS EPITHELIUM CELL; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; CELL CULTURE; DIABETIC NEPHROPATHIES; DRUG EFFECTS; GLUCOSE BLOOD LEVEL; METABOLISM; PATHOLOGY; PROTECTION; UROTHELIUM;

BLOOD GLUCOSE; CELLS, CULTURED; DIABETIC NEPHROPATHIES; GLUCOSE TRANSPORTER TYPE 1; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HUMANS; PEPTIDE FRAGMENTS; PROTECTIVE FACTORS; PROTEIN KINASE C; TRYPTOPHAN; UROTHELIUM;

EID: 84980039405     PISSN: 03011623     EISSN: 15732584     Source Type: Journal    
DOI: 10.1007/s11255-016-1377-x     Document Type: Article

References (32)

1. Forbes JM, Cooper ME (2013) Mechanisms of diabetic complications. Physiol Rev 93(1):137–188. doi:10.1152/physrev.00045.2011
2. Sena CM, Pereira AM, Seica R (2013) Endothelial dysfunction—a major mediator of diabetic vascular disease. Biochim Biophys Acta 1832(12):2216–2231. doi:10.1016/j.bbadis.2013.08.006
3. Burrows NR, Li Y, Geiss LS (2010) Incidence of treatment for end-stage renal disease among individuals with diabetes in the U.S. continues to decline. Diabetes Care 33(1):73–77. doi:10.2337/dc09-0343
4. Gerstein HC, Mann JF, Yi Q, Zinman B, Dinneen SF, Hoogwerf B, Halle JP, Young J, Rashkow A, Joyce C, Nawaz S, Yusuf S, Investigators HS (2001) Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA 286(4):421–426
5. Eleftheriadis T, Antoniadi G, Pissas G, Liakopoulos V, Stefanidis I (2013) The renal endothelium in diabetic nephropathy. Ren Fail 35(4):592–599. doi:10.3109/0886022X.2013.773836
6. Brosius FC, Heilig CW (2005) Glucose transporters in diabetic nephropathy. Pediatr Nephrol 20(4):447–451. doi:10.1007/s00467-004-1748-x
7. Brownlee M (2005) The pathobiology of diabetic complications: a unifying mechanism. Diabetes 54(6):1615–1625
8. Castilho BA, Shanmugam R, Silva RC, Ramesh R, Himme BM, Sattlegger E (2014) Keeping the eIF2 alpha kinase Gcn2 in check. Biochim Biophys Acta 1843(9):1948–1968. doi:10.1016/j.bbamcr.2014.04.006
9. Laeger T, Henagan TM, Albarado DC, Redman LM, Bray GA, Noland RC, Munzberg H, Hutson SM, Gettys TW, Schwartz MW, Morrison CD (2014) FGF21 is an endocrine signal of protein restriction. J Clin Investig 124(9):3913–3922. doi:10.1172/JCI74915
10. Walker JD, Bending JJ, Dodds RA, Mattock MB, Murrells TJ, Keen H, Viberti GC (1989) Restriction of dietary protein and progression of renal failure in diabetic nephropathy. Lancet 2(8677):1411–1415
11. Zeller K, Whittaker E, Sullivan L, Raskin P, Jacobson HR (1991) Effect of restricting dietary protein on the progression of renal failure in patients with insulin-dependent diabetes mellitus. N Engl J Med 324(2):78–84. doi:10.1056/NEJM199101103240202
12. Eleftheriadis T, Pissas G, Antoniadi G, Liakopoulos V, Tsogka K, Sounidaki M, Stefanidis I (2016) Differential effects of the two amino acid sensing systems, the GCN2 kinase and the mTOR complex 1, on primary human alloreactive CD4 + T-cells. Int J Mol Med 37(5):1412–1420. doi:10.3892/ijmm.2016.2547
13. Eleftheriadis T, Pissas G, Antoniadi G, Spanoulis A, Liakopoulos V, Stefanidis I (2014) Indoleamine 2,3-dioxygenase increases p53 levels in alloreactive human T cells, and both indoleamine 2,3-dioxygenase and p53 suppress glucose uptake, glycolysis and proliferation. Int Immunol 26(12):673–684. doi:10.1093/intimm/dxu077
14. Jiang HY, Wek SA, McGrath BC, Scheuner D, Kaufman RJ, Cavener DR, Wek RC (2003) Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-kappaB in response to diverse cellular stresses. Mol Cell Biol 23(16):5651–5663
15. Eleftheriadis T, Pissas G, Yiannaki E, Markala D, Arampatzis S, Antoniadi G, Liakopoulos V, Stefanidis I (2013) Inhibition of indoleamine 2,3-dioxygenase in mixed lymphocyte reaction affects glucose influx and enzymes involved in aerobic glycolysis and glutaminolysis in alloreactive T-cells. Hum Immunol 74(12):1501–1509. doi:10.1016/j.humimm.2013.08.268
16. Du X, Matsumura T, Edelstein D, Rossetti L, Zsengeller Z, Szabo C, Brownlee M (2003) Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells. J Clin Investig 112(7):1049–1057. doi:10.1172/JCI18127
17. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404(6779):787–790. doi:10.1038/35008121
18. Gabbay KH, Merola LO, Field RA (1966) Sorbitol pathway: presence in nerve and cord with substrate accumulation in diabetes. Science 151(3707):209–210
19. Koya D, Jirousek MR, Lin YW, Ishii H, Kuboki K, King GL (1997) Characterization of protein kinase C beta isoform activation on the gene expression of transforming growth factor-beta, extracellular matrix components, and prostanoids in the glomeruli of diabetic rats. J Clin Investig 100(1):115–126. doi:10.1172/JCI119503
20. Kuboki K, Jiang ZY, Takahara N, Ha SW, Igarashi M, Yamauchi T, Feener EP, Herbert TP, Rhodes CJ, King GL (2000) Regulation of endothelial constitutive nitric oxide synthase gene expression in endothelial cells and in vivo: a specific vascular action of insulin. Circulation 101(6):676–681
21. Koya D, Haneda M, Nakagawa H, Isshiki K, Sato H, Maeda S, Sugimoto T, Yasuda H, Kashiwagi A, Ways DK, King GL, Kikkawa R (2000) Amelioration of accelerated diabetic mesangial expansion by treatment with a PKC beta inhibitor in diabetic db/db mice, a rodent model for type 2 diabetes. FASEB J Off Publ Fed Am Soc Exp Biol 14(3):439–447
22. Kolm-Litty V, Sauer U, Nerlich A, Lehmann R, Schleicher ED (1998) High glucose-induced transforming growth factor beta1 production is mediated by the hexosamine pathway in porcine glomerular mesangial cells. J Clin Investig 101(1):160–169. doi:10.1172/JCI119875
23. Wells L, Hart GW (2003) O-GlcNAc turns twenty: functional implications for post-translational modification of nuclear and cytosolic proteins with a sugar. FEBS Lett 546(1):154–158
24. Du XL, Edelstein D, Rossetti L, Fantus IG, Goldberg H, Ziyadeh F, Wu J, Brownlee M (2000) Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc Natl Acad Sci USA 97(22):12222–12226. doi:10.1073/pnas.97.22.12222
25. Du XL, Edelstein D, Dimmeler S, Ju Q, Sui C, Brownlee M (2001) Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J Clin Investig 108(9):1341–1348. doi:10.1172/JCI11235
26. Queisser MA, Yao D, Geisler S, Hammes HP, Lochnit G, Schleicher ED, Brownlee M, Preissner KT (2010) Hyperglycemia impairs proteasome function by methylglyoxal. Diabetes 59(3):670–678. doi:10.2337/db08-1565
27. Giacco F, Du X, D’Agati VD, Milne R, Sui G, Geoffrion M, Brownlee M (2014) Knockdown of glyoxalase 1 mimics diabetic nephropathy in nondiabetic mice. Diabetes 63(1):291–299. doi:10.2337/db13-0316
28. Brouwers O, Niessen PM, Miyata T, Ostergaard JA, Flyvbjerg A, Peutz-Kootstra CJ, Sieber J, Mundel PH, Brownlee M, Janssen BJ, De Mey JG, Stehouwer CD, Schalkwijk CG (2014) Glyoxalase-1 overexpression reduces endothelial dysfunction and attenuates early renal impairment in a rat model of diabetes. Diabetologia 57(1):224–235. doi:10.1007/s00125-013-3088-5
29. Sato S, Kawamura H, Takemoto M, Maezawa Y, Fujimoto M, Shimoyama T, Koshizaka M, Tsurutani Y, Watanabe A, Ueda S, Halevi K, Saito Y, Yokote K (2009) Halofuginone prevents extracellular matrix deposition in diabetic nephropathy. Biochem Biophys Res Commun 379(2):411–416. doi:10.1016/j.bbrc.2008.12.088
30. Pines M, Spector I (2015) Halofuginone—the multifaceted molecule. Molecules 20(1):573–594. doi:10.3390/molecules20010573
31. Passariello N, Sepe J, Marrazzo G, De Cicco A, Peluso A, Pisano MC, Sgambato S, Tesauro P, D’Onofrio F (1993) Effect of aldose reductase inhibitor (tolrestat) on urinary albumin excretion rate and glomerular filtration rate in IDDM subjects with nephropathy. Diabetes Care 16(5):789–795
32. Cherney DZ, Konvalinka A, Zinman B, Diamandis EP, Soosaipillai A, Reich H, Lorraine J, Lai V, Scholey JW, Miller JA (2009) Effect of protein kinase Cbeta inhibition on renal hemodynamic function and urinary biomarkers in humans with type 1 diabetes: a pilot study. Diabetes Care 32(1):91–93. doi:10.2337/dc08-1609