MicroRNA-29a Promotion of nephrin acetylation ameliorates hyperglycemia-induced podocyte dysfunction

Journal of the American Society of Nephrology

Volumn 25, Issue 8, 2014, Pages 1698-1709

  Lin, Chun Liang ^a,d   Lee, Pei Hsien ^a   Hsu, Yung Chien ^a   Lei, Chen Chou ^a   Ko, Jih Yang ^a   Chuang, Pei Chin ^a   Huang, Yu Ting ^a   Wang, Shao Yu ^a   Wu, Shin Long ^a   Chen, Yu Shan ^a   Chiang, Wen Chih ^b   Reiser, Jochen ^c   Wang, Feng Sheng ^a,e  

^a CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c RUSH UNIVERSITY MEDICAL CENTER   (United States)

^d CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^e College of Medicine ^*

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; GLUCOSE; HISTONE DEACETYLASE 4; HISTONE H3; MICRORNA 29A; NEPHRIN; HISTONE; HISTONE DEACETYLASE; MEMBRANE PROTEIN; MICRORNA; MIRN29 MICRORNA, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL VIABILITY; CONTROLLED STUDY; DEACETYLATION; DISEASE ASSOCIATION; ENRICHMENT CULTURE; GENE SILENCING; GLOMERULUS; HISTONE UBIQUITINATION; HOMEOSTASIS; HYPERGLYCEMIA; IN VITRO STUDY; INFLAMMATION; KIDNEY DYSFUNCTION; KIDNEY FUNCTION; MOUSE; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEINURIA; REGULATORY MECHANISM; RENAL PROTECTION; SIGNAL TRANSDUCTION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; URINARY EXCRETION; ACETYLATION; ANIMAL; DIABETES MELLITUS, EXPERIMENTAL; MALE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ACETYLATION; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; HISTONE DEACETYLASES; HISTONES; HYPERGLYCEMIA; MALE; MEMBRANE PROTEINS; MICE, TRANSGENIC; MICRORNAS; PODOCYTES; SIGNAL TRANSDUCTION;

EID: 84921677205     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2013050527     Document Type: Article

References (47)

1. Yuen DA, Stead BE, Zhang Y, White KE, Kabir MG, Thai K, Advani SL, Connelly KA, Takano T, Zhu L, Cox AJ, Kelly DJ, Gibson IW, Takahashi T, Harris RC, Advani A: eNOS deficiency predisposes podocytes to injury in diabetes. J Am Soc Nephrol 23: 1810-1823, 2012
2. Dai C, Stolz DB, Kiss LP, Monga SP, Holzman LB, Liu Y:Wnt/beta-catenin signaling promotes podocyte dysfunction and albuminuria. J Am Soc Nephrol 20: 1997-2008, 2009
3. Herman-EdelsteinM, ThomasMC, Thallas-Bonke V, SaleemM, Cooper ME, Kantharidis P: Dedifferentiation of immortalized human podocytes in response to transforming growth factor-b: A model for diabetic podocytopathy. Diabetes 60: 1779-1788, 2011
4. Wang H, Madhusudhan T, He T, Hummel B, Schmidt S, Vinnikov IA, Shahzad K, Kashif M, Muller-Krebs S, Schwenger V, Bierhaus A, Rudofsky G, Nawroth PP, Isermann B: Low but sustained coagulation activation ameliorates glucose-induced podocyte apoptosis: Protective effect of factor V Leiden in diabetic nephropathy. Blood 117: 5231-5242, 2011
5. Mima A, KitadaM, Geraldes P, LiQ, MatsumotoM,Mizutani K,QiW, Li C, Leitges M, Rask-Madsen C, King GL: Glomerular VEGF resistance induced by PKCd/SHP-1 activation and contribution to diabetic nephropathy. FASEB J 26: 2963-2974, 2012
6. Wang W,Wang Y, Long J,Wang J, Haudek SB,Overbeek P, Chang BH, Schumacker PT, Danesh FR: Mitochondrial fission triggered by hyperglycemia is mediated by ROCK1 activation in podocytes and endothelial cells. Cell Metab 15: 186-200, 2012
7. Welsh GI, Saleem MA: Nephrin-signature molecule of the glomerular podocyte? J Pathol 220: 328-337, 2010
8. Hussain S, Romio L, SaleemM,Mathieson P, Serrano M, Moscat J, Diaz-MecoM, Scambler P, Koziell A: Nephrin deficiency activates NF-kappaB and promotes glomerular injury. J Am Soc Nephrol 20: 1733-1743, 2009
9. Inoki K, Mori H, Wang J, Suzuki T, Hong S, Yoshida S, Blattner SM, Ikenoue T, Rüegg MA, Hall MN, Kwiatkowski DJ, Rastaldi MP, Huber TB, KretzlerM, Holzman LB,Wiggins RC, Guan KL: mTORC1 activation in podocytes is a critical step in the development of diabetic nephropathy in mice. J Clin Invest 121: 2181-2196, 2011
10. Liu W, Zhang Y, Hao J, Liu S, Liu Q, Zhao S, Shi Y, Duan H: Nestin protects mouse podocytes against high glucose-induced apoptosis by a Cdk5-dependent mechanism. J Cell Biochem 113: 3186-3196, 2012
11. Qin XS, Tsukaguchi H, Shono A, Yamamoto A, Kurihara H, Doi T: Phosphorylation of nephrin triggers its internalization by raft-mediated endocytosis. J Am Soc Nephrol 20: 2534-2545, 2009
12. Tossidou I, Teng B, Drobot L, Meyer-Schwesinger C, Worthmann K, Haller H, Schiffer M: CIN85/RukL is a novel binding partner of nephrin and podocin andmediates slit diaphragmturnover in podocytes. J Biol Chem 285: 25285-25295, 2010
13. Weinhold B, Sellmeier M, Schaper W, Blume L, Philippens B, Kats E, Bernard U, Galuska SP, Geyer H, Geyer R, Worthmann K, Schiffer M, Groos S, Gerardy-Schahn R, Münster-Kühnel AK: Deficits in sialylation impair podocyte maturation. J Am Soc Nephrol 23: 1319-1328, 2012
14. Quack I,WoznowskiM, Potthoff SA, Palmer R, Königshausen E, Sivritas S, Schiffer M, Stegbauer J, Vonend O, Rump LC, Sellin L: PKC alpha mediates beta-arrestin2-dependent nephrin endocytosis in hyperglycemia. J Biol Chem 286: 12959-12970, 2011
15. Mihaylova MM, Vasquez DS, Ravnskjaer K, Denechaud PD, Yu RT, Alvarez JG, Downes M, Evans RM, Montminy M, Shaw RJ: Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 145: 607-621, 2011
16. Sando R 3rd, Gounko N, Pieraut S, Liao L, Yates J 3rd, Maximov A: HDAC4 governs a transcriptional program essential for synaptic plasticity and memory. Cell 151: 821-834, 2012
17. Li J, Chen J, Ricupero CL, Hart RP, SchwartzMS, Kusnecov A, Herrup K: Nuclear accumulation of HDAC4 in ATM deficiency promotes neurodegeneration in ataxia telangiectasia. Nat Med 18: 783-790, 2012
18. Yuan JH, Yang F, Chen BF, Lu Z, Huo XS, Zhou WP, Wang F, Sun SH: The histone deacetylase 4/SP1/microrna-200a regulatory network contributes to aberrant histone acetylation in hepatocellular carcinoma. Hepatology 54: 2025-2035, 2011
19. Van Beneden K, Geers C, Pauwels M, Mannaerts I, Verbeelen D, van Grunsven LA, Van den Branden C: Valproic acid attenuates proteinuria and kidney injury. J Am Soc Nephrol 22: 1863-1875, 2011
20. Gilbert RE, Huang Q, Thai K, Advani SL, Lee K, Yuen DA, Connelly KA, Advani A: Histone deacetylase inhibition attenuates diabetes-associated kidney growth: Potential role for epigeneticmodification of the epidermal growth factor receptor. Kidney Int 79: 1312-1321, 2011
21. Esteller M: Non-coding RNAs in human disease. Nat Rev Genet 12: 861-874, 2011
22. Krupa A, Jenkins R, Luo DD, Lewis A, Phillips A, Fraser D: Loss of MicroRNA-192 promotes fibrogenesis in diabetic nephropathy.J AmSoc Nephrol 21: 438-447, 2010
23. Qin W, Chung AC, Huang XR, Meng XM, Hui DS, Yu CM, Sung JJ, Lan HY: TGF-b/Smad3 signaling promotes renal fibrosis by inhibiting miR-29. J Am Soc Nephrol 22: 1462-1474, 2011
24. Winbanks CE, Wang B, Beyer C, Koh P, White L, Kantharidis P, Gregorevic P: TGF-beta regulates miR-206 and miR-29 to control myogenic differentiation through regulation of HDAC4. J Biol Chem 286: 13805-13814, 2011
25. Liu S, Wu LC, Pang J, Santhanam R, Schwind S,Wu YZ, Hickey CJ, Yu J, Becker H, Maharry K, Radmacher MD, Li C, Whitman SP, Mishra A, Stauffer N, Eiring AM, Briesewitz R, Baiocchi RA, Chan KK, Paschka P, CaligiuriMA, Byrd JC, Croce CM, Bloomfield CD, Perrotti D, Garzon R, MarcucciG: Sp1/NFkappaB/HDAC/miR-29b regulatory network in KITdriven myeloid leukemia. Cancer Cell 17: 333-347, 2010
26. Lin CL,Wang FS, Hsu YC, Chen CN, Tseng MJ, Saleem MA, Chang PJ, Wang JY: Modulation of notch-1 signaling alleviates vascular endothelial growth factor-mediated diabetic nephropathy. Diabetes 59: 1915-1925, 2010
27. PichaiwongW, Hudkins KL, Wietecha T, Nguyen TQ, Tachaudomdach C, Li W, Askari B, Kobayashi T, O'Brien KD, Pippin JW, Shankland SJ, Alpers CE: Reversibility of structural and functional damage in a model of advanced diabetic nephropathy. J Am Soc Nephrol 24: 1088-1102, 2013
28. Du B,Ma LM, HuangMB, Zhou H, Huang HL, Shao P, Chen YQ, Qu LH: High glucose down-regulates miR-29a to increase collagen IV production in HK-2 cells. FEBS Lett 584: 811-816, 2010
29. Wang XH, Hu Z, Klein JD, Zhang L, Fang F, Mitch WE: Decreased miR-29 suppresses myogenesis in CKD. J AmSocNephrol 22: 2068-2076, 2011
30. Wang B, Komers R, Carew R,Winbanks CE, Xu B, Herman-EdelsteinM, Koh P, Thomas M, Jandeleit-Dahm K, Gregorevic P, Cooper ME, Kantharidis P: Suppression of microRNA-29 expression by TGF-b1 promotes collagen expression and renal fibrosis. J AmSocNephrol 23: 252-265, 2012
31. Long J, Wang Y, Wang W, Chang BH, 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 Chem286: 11837-11848, 2011
32. Wang G, Kwan BC, Lai FM, Chow KM, Li PK, Szeto CC: Urinary miR-21, miR-29, and miR-93: Novel biomarkers of fibrosis. Am J Nephrol 36: 412-418, 2012
33. George B, Verma R, Soofi AA, Garg P, Zhang J, Park TJ, Giardino L, Ryzhova L, Johnstone DB, Wong H, Nihalani D, Salant DJ, Hanks SK, Curran T, Rastaldi MP, Holzman LB: Crk1/2-dependent signaling is necessary for podocyte foot process spreading in mouse models of glomerular disease. J Clin Invest 122: 674-692, 2012
34. Kajiho Y, Harita Y, Kurihara H, Horita S,Matsunaga A, Tsurumi H, Kanda S, Sugawara N, Miura K, Sekine T, Hattori S, HattoriM, Igarashi T: SIRPa interacts with nephrin at the podocyte slit diaphragm. FEBS J 279: 3010-3021, 2012
35. Chen S, Bellew C, Yao X, Stefkova J, Dipp S, Saifudeen Z, Bachvarov D, El-Dahr SS:Histone deacetylase (HDAC) activity is critical for embryonic kidney gene expression, growth, and differentiation. J Biol Chem286: 32775-32789, 2011
36. Geng H, Harvey CT, Pittsenbarger J, Liu Q, Beer TM, Xue C, Qian DZ: HDAC4 protein regulates HIF1a protein lysine acetylation and cancer cell response to hypoxia. J Biol Chem 286: 38095-38102, 2011
37. Anokye-Danso F, TrivediCM, JuhrD,Gupta M,Cui Z, Tian Y, Zhang Y, Yang W, Gruber PJ, Epstein JA, Morrisey EE: Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 8: 376-388, 2011
38. Rivetti di Val Cervo P, Lena AM, Nicoloso M, Rossi S, Mancini M, Zhou H, Saintigny G, Dellambra E, Odorisio T, Mahe C, Calin GA, Candi E, Melino G: p63-microRNA feedback in kerationcyte senescence. Proc Natl Acad Sci U S A 109: 1133-1138, 2012
39. Sampath D, Liu C, Vasan K, SuldaM, Puduvalli VK, WierdaWG, Keating MJ: Histone deacetylases mediate the silencing of miR-15a, miR-16, and miR-29b in chronic lymphocytic leukemia. Blood 119: 1162-1172, 2012
40. Qi Z, Fujita H, Jin J, Davis LS, Wang Y, Fogo AB, Breyer MD: Characterization of susceptibility of inbred mouse strains to diabetic nephropathy. Diabetes 54: 2628-2637, 2005
41. Lin CL, Wang JY, Ko JY, Huang YT, Kuo YH, Wang FS: Dickkopf-1 promotes hyperglycemia-induced accumulation of mesangial matrix and renal dysfunction. J Am Soc Nephrol 21: 124-135, 2010
42. Hsiao YC, Chang HH, Tsai CY, Jong YJ, Horng LS, Lin SF, Tsai TF: Coat color-tagged green mouse with EGFP expressed from the RNA polymerase II promoter. Genesis 39: 122-129, 2004
43. TakemotoM, Asker N, Gerhardt H, Lundkvist A, Johansson BR, Saito Y, Betsholtz C: A new method for large scale isolation of kidney glomeruli from mice. Am J Pathol 161: 799-805, 2002
44. Golos M, Lewko B, Bryl E,Witkowski JM, Dubaniewicz A, Olszewska A, Latawiec E, Angielski S, Stepinski J: Effect of angiotensin II on ANPdependent guanylyl cyclase activity in cultured mouse and rat podocytes. Kidney Blood Press Res 25: 296-302, 2002
45. Ko JY, Wu RW, Kuo SJ, Chen MW, Yeh DW, Ke HC, Wu SL, Wang FS: Cannabinoid receptor 1 mediates glucocorticoid-induced bone loss in rats by perturbing bone mineral acquisition and marrow adipogenesis. Arthritis Rheum 64: 1204-1214, 2012
46. Mundel P, Reiser J, Zúñiga Mejía Borja A, Pavenstädt H, Davidson GR, Kriz W, Zeller R: 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, 1997
47. de Medeiros RB: Sequential chromatin immunoprecipitation assay and analysis. Methods Mol Biol 791: 225-237, 2011