Overexpression of miR-34c inhibits high glucose-induced apoptosis in podocytes by targeting Notch signaling pathways

International Journal of Clinical and Experimental Pathology

Volumn 8, Issue 5, 2015, Pages 4525-4534

  Liu, Xiang Dong ^a   Zhang, Lian Yun ^a   Zhu, Tie Chui ^a   Zhang, Rui Fang ^a   Wang, Shu Long ^a   Bao, Yan ^a  

^a XINXIANG MEDICAL UNIVERSITY   (China)

Author keywords

Cell apoptosis; Diabetic nephropathy; MicroRNAs; Notch; Podocytes

Indexed keywords

3' UNTRANSLATED REGION; APOPTOSIS REGULATORY PROTEIN; CALCIUM BINDING PROTEIN; GLUCOSE; JAG1 PROTEIN, MOUSE; MEMBRANE PROTEIN; MICRORNA; MIRN34 MICRORNA, MOUSE; NOTCH1 PROTEIN, MOUSE; NOTCH1 RECEPTOR; PROTEIN JAGGED 1; SERRATE JAGGED PROTEIN; SIGNAL PEPTIDE;

3' UNTRANSLATED REGION; ANIMAL; APOPTOSIS; BINDING SITE; DIABETIC NEPHROPATHY; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; METABOLISM; MOUSE; PATHOLOGY; PODOCYTE; SIGNAL TRANSDUCTION; TIME FACTOR; TRANSFORMED CELL LINE; UPREGULATION;

3' UNTRANSLATED REGIONS; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BINDING SITES; CALCIUM-BINDING PROTEINS; CELL LINE, TRANSFORMED; DIABETIC NEPHROPATHIES; GLUCOSE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; JAGGED-1 PROTEIN; MEMBRANE PROTEINS; MICE; MICRORNAS; PODOCYTES; RECEPTOR, NOTCH1; SERRATE-JAGGED PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; UP-REGULATION;

EID: 84937852680     PISSN: None     EISSN: 19362625     Source Type: Journal    
DOI: None     Document Type: Article

References (41)

1. Nakai S, Masakane I, Akiba T, Shigematsu T, Yamagata K, Watanabe Y, Iseki K, Itami N, Shinoda T, Morozumi K, Shoji T, Marubayashi S, Morita O, Kimata N, Suzuki K, Tsuchida K, Nakamoto H, Hamano T, Yamashita A, Wakai K, Wada A and Tsubakihara Y. Overview of regular dialysis treatment in Japan as of 31 December 2006. Ther Apher Dial 2008; 12: 428-456.
2. Yoon KH, Lee JH, Kim JW, Cho JH, Choi YH, Ko SH, Zimmet P and Son HY. Epidemic obesity and type 2 diabetes in Asia. Lancet 2006; 368: 1681-1688.
3. Coimbra TM, Janssen U, Grone HJ, Ostendorf T, Kunter U, Schmidt H, Brabant G and Floege J. Early events leading to renal injury in obese Zucker (fatty) rats with type II diabetes. Kidney Int 2000; 57: 167-182.
4. Siu B, Saha J, Smoyer WE, Sullivan KA and Brosius FC 3rd. Reduction in podocyte density as a pathologic feature in early diabetic nephropathy in rodents: prevention by lipoic acid treatment. BMC Nephrol 2006; 7: 6.
5. Li CX, Xia M, Han WQ, Li XX, Zhang C, Boini KM, Liu XC and Li PL. Reversal by growth hormone of homocysteine-induced epithelial-to-mesenchymal transition through membrane raft-redox signaling in podocytes. Cell Physiol Biochem 2011; 27: 691-702.
6. Riediger F, Quack I, Qadri F, Hartleben B, Park JK, Potthoff SA, Sohn D, Sihn G, Rousselle A, Fokuhl V, Maschke U, Purfurst B, Schneider W, Rump LC, Luft FC, Dechend R, Bader M, Huber TB, Nguyen G and Muller DN. Prorenin receptor is essential for podocyte autophagy and survival. J Am Soc Nephrol 2011; 22: 2193-2202.
7. Susztak K, Raff AC, Schiffer M and Bottinger EP. Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes 2006; 55: 225-233.
8. Steffes MW, Schmidt D, McCrery R and Basgen JM. Glomerular cell number in normal subjects and in type 1 diabetic patients. Kidney Int 2001; 59: 2104-2113.
9. Yuan H, Ren ZL, Hu FQ, Liang W and Ding GH. Renin induces apoptosis in podocytes through a receptor-mediated, angiotensin II-indepen-dent mechanism. Am J Med Sci 2012; 344: 441-446.
10. Kim KM, Kim YS, Jung DH, Lee J and Kim JS. Increased glyoxalase I levels inhibit accumulation of oxidative stress and an advanced glycation end product in mouse mesangial cells cultured in high glucose. Exp Cell Res 2012; 318: 152-159.
11. Lim JC, Lim SK, Park MJ, Kim GY, Han HJ and Park SH. Cannabinoid receptor 1 mediates high glucose-induced apoptosis via endoplasmic reticulum stress in primary cultured rat mesangial cells. Am J Physiol Renal Physiol 2011; 301: 16.
12. Chen J, Gui D, Chen Y, Mou L, Liu Y and Huang J. Astragaloside IV improves high glucose-induced podocyte adhesion dysfunction via alpha3beta1 integrin upregulation and integrin-linked kinase inhibition. Biochem Pharmacol 2008; 76: 796-804.
13. Walsh DW, Roxburgh SA, McGettigan P, Berthier CC, Higgins DG, Kretzler M, Cohen CD, Mezzano S, Brazil DP and Martin F. Co-regulation of Gremlin and Notch signalling in diabetic nephropathy. Biochim Biophys Acta 2008; 1: 10-21.
14. Cook KM and Figg WD. Angiogenesis inhibitors: current strategies and future prospects. CA Cancer J Clin 2010; 60: 222-243.
15. Ji X, Wang Z, Geamanu A, Sarkar FH and Gupta SV. Inhibition of cell growth and induction of apoptosis in non-small cell lung cancer cells by delta-tocotrienol is associated with notch-1 down-regulation. J Cell Biochem 2011; 112: 2773-2783.
16. Hilton MJ, Tu X, Wu X, Bai S, Zhao H, Kobayashi T, Kronenberg HM, Teitelbaum SL, Ross FP, Kopan R and Long F. Notch signaling maintains bone marrow mesenchymal progenitors by suppressing osteoblast differentiation. Nat Med 2008; 14: 306-314.
17. Samon JB, Champhekar A, Minter LM, Telfer JC, Miele L, Fauq A, Das P, Golde TE and Osborne BA. Notch1 and TGFbeta1 cooperatively regulate Foxp3 expression and the maintenance of peripheral regulatory T cells. Blood 2008; 112: 1813-1821.
18. McCright B. Notch signaling in kidney development. Curr Opin Nephrol Hypertens 2003; 12: 5-10.
19. Hayward P, Kalmar T and Arias AM. Wnt/Notch signalling and information processing during development. Development 2008; 135: 411-424.
20. Lin CL, Wang FS, Hsu YC, Chen CN, Tseng MJ, Saleem MA, Chang PJ and Wang JY. Modulation of notch-1 signaling alleviates vascular endothelial growth factor-mediated diabetic nephropathy. Diabetes 2010; 59: 1915-1925.
21. Bonegio R and Susztak K. Notch signaling in diabetic nephropathy. Exp Cell Res 2012; 318: 986-992.
22. Mendell JT and Olson EN. MicroRNAs in stress signaling and human disease. Cell 2012; 148: 1172-1187.
23. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116: 281-297.
24. Winter J, Jung S, Keller S, Gregory RI and Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 2009; 11: 228-234.
25. Zhdanova O, Srivastava S, Di L, Li Z, Tchelebi L, Dworkin S, Johnstone DB, Zavadil J, Chong MM, Littman DR, Holzman LB, Barisoni L and Skolnik EY. The inducible deletion of Drosha and microRNAs in mature podocytes results in a collapsing glomerulopathy. Kidney Int 2011; 80: 719-730.
26. Harvey SJ, Jarad G, Cunningham J, Goldberg S, Schermer B, Harfe BD, McManus MT, Benzing T and Miner JH. Podocyte-specific deletion of dicer alters cytoskeletal dynamics and causes glomerular disease. J Am Soc Nephrol 2008; 19: 2150-2158.
27. Shi S, Yu L, Chiu C, Sun Y, Chen J, Khitrov G, Merkenschlager M, Holzman LB, Zhang W, Mundel P and Bottinger EP. Podocyte-selective deletion of dicer induces proteinuria and glomerulosclerosis. J Am Soc Nephrol 2008; 19: 2159-2169.
28. Ho J, Ng KH, Rosen S, Dostal A, Gregory RI and Kreidberg JA. Podocyte-specific loss of functional microRNAs leads to rapid glomerular and tubular injury. J Am Soc Nephrol 2008; 19: 2069-2075.
29. Long J, Wang Y, Wang W, Chang BH and Danesh FR. Identification of microRNA-93 as a novel regulator of vascular endothelial growth factor in hyperglycemic conditions. J Biol Chem 2010; 285: 23457-23465.
30. Long J, Wang Y, Wang W, Chang BH and Danesh FR. MicroRNA-29c is a signature microRNA under high glucose conditions that targets Sprouty homolog 1, and its in vivo knockdown prevents progression of diabetic nephropathy. J Biol Chem 2011; 286: 11837-11848.
31. Lanford RE, Hildebrandt-Eriksen ES, Petri A, Persson R, Lindow M, Munk ME, Kauppinen S and Orum H. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 2010; 327: 198-201.
32. Gao F, Yao M, Shi Y, Hao J, Ren Y, Liu Q, Wang X and Duan H. Notch pathway is involved in high glucose-induced apoptosis in podocytes via Bcl-2 and p53 pathways. J Cell Biochem 2013; 114: 1029-1038.
33. Saleem MA, O'Hare MJ, Reiser J, Coward RJ, Inward CD, Farren T, Xing CY, Ni L, Mathieson PW and Mundel P. A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression. J Am Soc Nephrol 2002; 13: 630-638.
34. Morizane R, Fujii S, Monkawa T, Hiratsuka K, Yamaguchi S, Homma K and Itoh H. miR-34c attenuates epithelial-mesenchymal transition and kidney fibrosis with ureteral obstruction. Sci Rep 2014; 4: 4578.
35. Niranjan T, Bielesz B, Gruenwald A, Ponda MP, Kopp JB, Thomas DB and Susztak K. The Notch pathway in podocytes plays a role in the development of glomerular disease. Nat Med 2008; 14: 290-298.
36. Liu L, Gao C, Chen G, Li X, Li J, Wan Q and Xu Y. Notch Signaling Molecules Activate TGF-beta in Rat Mesangial Cells under High Glucose Conditions. J Diabetes Res 2013; 2013: 979702.
37. Kim D, Lim S, Park M, Choi J, Kim J, Han H, Yoon K, Kim K, Lim J and Park S. Ubiquitination-dependent CARM1 degradation facilitates Notch1-mediated podocyte apoptosis in diabetic nephropathy. Cell Signal 2014; 26: 1774-1782.
38. Bae Y, Yang T, Zeng HC, Campeau PM, Chen Y, Bertin T, Dawson BC, Munivez E, Tao J and Lee BH. miRNA-34c regulates Notch signaling during bone development. Hum Mol Genet 2012; 21: 2991-3000.
39. Catuogno S, Cerchia L, Romano G, Pognonec P, Condorelli G and de Franciscis V. miR-34c may protect lung cancer cells from paclitaxel-induced apoptosis. Oncogene 2013; 32: 341-351.
40. Liang X, Zhou D, Wei C, Luo H, Liu J, Fu R and Cui S. MicroRNA-34c enhances murine male germ cell apoptosis through targeting ATF1. PLoS One 2012; 7: 30.
41. Hagman Z, Larne O, Edsjo A, Bjartell A, Ehrnstrom RA, Ulmert D, Lilja H and Ceder Y. miR-34c is downregulated in prostate cancer and exerts tumor suppressive functions. Int J Cancer 2010; 127: 2768-2776.