Alteration of forkhead box o (foxo4) acetylation mediates apoptosis of podocytes in diabetes mellitus

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Chuang, Peter Y ^a   Dai, Yan ^a,b   Liu, Ruijie ^c   He, Helen ^a   Kretzler, Matthias ^d   Jim, Belinda ^e   Cohen, Clemens D ^f   He, John C ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b SHANGHAI FIRST PEOPLE S HOSPITAL   (China)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

SIRTUIN 1; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR FOXO4; UNCLASSIFIED DRUG; ADVANCED GLYCATION END PRODUCT; APOPTOSIS REGULATORY PROTEIN; BCL 2 LIKE PROTEIN 11; BCL-2-LIKE PROTEIN 11; BOVINE SERUM ALBUMIN; FORKHEAD TRANSCRIPTION FACTOR; FOXO4 PROTEIN, MOUSE; MEMBRANE PROTEIN; ONCOPROTEIN; SIRT1 PROTEIN, MOUSE;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BCL2L11 GENE; BINDING AFFINITY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DEACETYLATION; DIABETES MELLITUS; DIABETIC NEPHROPATHY; DOWN REGULATION; GENE; GENE ACTIVATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; GLOMERULUS; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PODOCYTE; PROTEIN BINDING; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE; ANIMAL; C57BL MOUSE; CATTLE; CELL CULTURE; CELL LINE; CHEMISTRY; DRUG EFFECT; GENE EXPRESSION; GENETICS; METABOLISM; MUTATION; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOLOGY; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING;

BOVINAE; MURINAE; MUS;

ACETYLATION; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BLOTTING, WESTERN; CATTLE; CELL LINE; CELLS, CULTURED; DIABETES MELLITUS; DIABETES MELLITUS, TYPE 2; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; KIDNEY GLOMERULUS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MUTATION; PODOCYTES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SERUM ALBUMIN, BOVINE; SIRTUIN 1;

EID: 80051750952     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023566     Document Type: Article

References (50)

1. Yamagishi S, Fukami K, Ueda S, Okuda S, (2007) Molecular mechanisms of diabetic nephropathy and its therapeutic intervention. Curr Drug Targets 8: 952-959.
2. 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.
3. Pagtalunan ME, Miller PL, Jumping-Eagle S, Nelson RG, Myers BD, et al. (1997) Podocyte loss and progressive glomerular injury in type II diabetes. J Clin Invest 99: 342-348.
4. Meyer TW, Bennett PH, Nelson RG, (1999) Podocyte number predicts long-term urinary albumin excretion in Pima Indians with Type II diabetes and microalbuminuria. Diabetologia 42: 1341-1344.
5. Dalla Vestra M, Masiero A, Roiter AM, Saller A, Crepaldi G, et al. (2003) Is podocyte injury relevant in diabetic nephropathy? Studies in patients with type 2 diabetes. Diabetes 52: 1031-1035.
6. Verzola D, Gandolfo MT, Ferrario F, Rastaldi MP, Villaggio B, et al. (2007) Apoptosis in the kidneys of patients with type II diabetic nephropathy. Kidney Int 72: 1262-1272.
7. 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.
8. Yoo TH, Li JJ, Kim JJ, Jung DS, Kwak SJ, et al. (2007) Activation of the renin-angiotensin system within podocytes in diabetes. Kidney Int 71: 1019-1027.
9. Chuang PY, Yu Q, Fang W, Uribarri J, He JC, (2007) Advanced glycation endproducts induce podocyte apoptosis by activation of the FOXO4 transcription factor. Kidney Int 72: 965-976.
10. Forbes JM, Cooper ME, Oldfield MD, Thomas MC, (2003) Role of advanced glycation end products in diabetic nephropathy. J Am Soc Nephrol 14: S254-258.
11. Furukawa-Hibi Y, Kobayashi Y, Chen C, Motoyama N, (2005) FOXO transcription factors in cell-cycle regulation and the response to oxidative stress. Antioxid Redox Signal 7: 752-760.
12. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, et al. (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303: 2011-2015.
13. Cai W, He JC, Zhu L, Lu C, Vlassara H, (2006) Advanced glycation end product (AGE) receptor 1 suppresses cell oxidant stress and activation signaling via EGF receptor. Proc Natl Acad Sci U S A 103: 13801-13806.
14. Moffat J, Grueneberg DA, Yang X, Kim SY, Kloepfer AM, et al. (2006) A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124: 1283-1298.
15. Rasband WS, (1997-2009) ImageJ Bethesda, Maryland, USA U.S. National Institutes of Health.
16. He JC, Husain M, Sunamoto M, D'Agati VD, Klotman ME, et al. (2004) Nef stimulates proliferation of glomerular podocytes through activation of Src-dependent Stat3 and MAPK1,2 pathways. J Clin Invest 114: 643-651.
17. Baelde JJ, Bergijk EC, Hoedemaeker PJ, de Heer E, Bruijn JA, (1994) Optimal method for RNA extraction from mouse glomeruli. Nephrol Dial Transplant 9: 304-308.
18. Lee TI, Johnstone SE, Young RA, (2006) Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat Protoc 1: 729-748.
19. Cohen CD, Klingenhoff A, Boucherot A, Nitsche A, Henger A, et al. (2006) Comparative promoter analysis allows de novo identification of specialized cell junction-associated proteins. Proc Natl Acad Sci U S A 103: 5682-5687.
20. Cohen CD, Lindenmeyer MT, Eichinger F, Hahn A, Seifert M, et al. (2008) Improved elucidation of biological processes linked to diabetic nephropathy by single probe-based microarray data analysis. PLoS One 3: e2937.
21. Motta MC, Divecha N, Lemieux M, Kamel C, Chen D, et al. (2004) Mammalian SIRT1 represses forkhead transcription factors. Cell 116: 551-563.
22. van der Horst A, Tertoolen LG, de Vries-Smits LM, Frye RA, Medema RH, et al. (2004) FOXO4 is acetylated upon peroxide stress and deacetylated by the longevity protein hSir2(SIRT1). J Biol Chem 279: 28873-28879.
23. Yan SF, Ramasamy R, Naka Y, Schmidt AM, (2003) Glycation, inflammation, and RAGE: a scaffold for the macrovascular complications of diabetes and beyond. Circ Res 93: 1159-1169.
24. Cohen CD, Frach K, Schlondorff D, Kretzler M, (2002) Quantitative gene expression analysis in renal biopsies: a novel protocol for a high-throughput multicenter application. Kidney Int 61: 133-140.
25. Bannister AJ, Miska EA, (2000) Regulation of gene expression by transcription factor acetylation. Cell Mol Life Sci 57: 1184-1192.
26. Gray SG, De Meyts P, (2005) Role of histone and transcription factor acetylation in diabetes pathogenesis. Diabetes Metab Res Rev 21: 416-433.
27. Niranjan T, Bielesz B, Gruenwald A, Ponda MP, Kopp JB, et al. (2008) The Notch pathway in podocytes plays a role in the development of glomerular disease. Nat Med 14: 290-298.
28. Menini S, Iacobini C, Oddi G, Ricci C, Simonelli P, et al. (2007) Increased glomerular cell (podocyte) apoptosis in rats with streptozotocin-induced diabetes mellitus: role in the development of diabetic glomerular disease. Diabetologia 50: 2591-2599.
29. Schiffer M, Bitzer M, Roberts IS, Kopp JB, ten Dijke P, et al. (2001) Apoptosis in podocytes induced by TGF-beta and Smad7. J Clin Invest 108: 807-816.
30. 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.
31. Berthier CC, Zhang H, Schin M, Henger A, Nelson RG, et al. (2009) Enhanced expression of Janus kinase-signal transducer and activator of transcription pathway members in human diabetic nephropathy. Diabetes 58: 469-477.
32. Kume S, Haneda M, Kanasaki K, Sugimoto T, Araki S, et al. (2006) Silent information regulator 2 (SIRT1) attenuates oxidative stress-induced mesangial cell apoptosis via p53 deacetylation. Free Radic Biol Med 40: 2175-2182.
33. You H, Mak TW, (2005) Crosstalk between p53 and FOXO transcription factors. Cell Cycle 4: 37-38.
34. van der Vos KE, Coffer PJ, (2008) FOXO-binding partners: it takes two to tango. Oncogene 27: 2289-2299.
35. Kume S, Haneda M, Kanasaki K, Sugimoto T, Araki S, et al. (2007) SIRT1 inhibits transforming growth factor beta-induced apoptosis in glomerular mesangial cells via Smad7 deacetylation. J Biol Chem 282: 151-158.
36. Dioum EM, Chen R, Alexander MS, Zhang Q, Hogg RT, et al. (2009) Regulation of hypoxia-inducible factor 2alpha signaling by the stress-responsive deacetylase sirtuin 1. Science 324: 1289-1293.
37. Nie Y, Erion DM, Yuan Z, Dietrich M, Shulman GI, et al. (2009) STAT3 inhibition of gluconeogenesis is downregulated by SirT1. Nat Cell Biol 11: 492-500.
38. Hao CM, Haase VH, (2010) Sirtuins and their relevance to the kidney. J Am Soc Nephrol 21: 1620-1627.
39. Zhang Q, Wang SY, Fleuriel C, Leprince D, Rocheleau JV, et al. (2007) Metabolic regulation of SIRT1 transcription via a HIC1:CtBP corepressor complex. Proc Natl Acad Sci U S A 104: 829-833.
40. Abdelmohsen K, Pullmann R Jr, Lal A, Kim HH, Galban S, et al. (2007) Phosphorylation of HuR by Chk2 regulates SIRT1 expression. Mol Cell 25: 543-557.
41. Yamakuchi M, Ferlito M, Lowenstein CJ, (2008) miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci U S A 105: 13421-13426.
42. Wautier MP, Chappey O, Corda S, Stern DM, Schmidt AM, et al. (2001) Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab 280: E685-694.
43. Liu D, Xu Y, (2010) p53, oxidative stress and aging Antioxid Redox Signal.
44. Giannakou ME, Partridge L, (2004) The interaction between FOXO and SIRT1: tipping the balance towards survival. Trends Cell Biol 14: 408-412.
45. Kume S, Uzu T, Horiike K, Chin-Kanasaki M, Isshiki K, et al. Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. J Clin Invest 120: 1043-1055.
46. Benigni A, Corna D, Zoja C, Sonzogni A, Latini R, et al. (2009) Disruption of the Ang II type 1 receptor promotes longevity in mice. J Clin Invest 119: 524-530.
47. Sharma S, Anjaneyulu M, Kulkarni SK, Chopra K, (2006) Resveratrol, a polyphenolic phytoalexin, attenuates diabetic nephropathy in rats. Pharmacology 76: 69-75.
48. Bordone L, Cohen D, Robinson A, Motta MC, van Veen E, et al. (2007) SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell 6: 759-767.
49. Banks AS, Kon N, Knight C, Matsumoto M, Gutierrez-Juarez R, et al. (2008) SirT1 gain of function increases energy efficiency and prevents diabetes in mice. Cell Metab 8: 333-341.
50. Zhao S, Xu W, Jiang W, Yu W, Lin Y, et al. (2010) Regulation of cellular metabolism by protein lysine acetylation. Science 327: 1000-1004.