Epigenetic changes in renal genes dysregulated in mouse and rat models of type 1 diabetes

Laboratory Investigation

Volumn 93, Issue 5, 2013, Pages 543-552

  Komers, Radko ^a   Mar, Daniel ^b   Denisenko, Oleg ^b   Xu, Bei ^a   Oyama, Terry T ^a   Bomsztyk, Karol ^b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

diabetic nephropathy; histone enzymes; histone modifications; RNA polymerase II

Indexed keywords

CALVASCULIN; CYCLOOXYGENASE 2; HISTONE DEMETHYLASE; HISTONE H3; LAMININ GAMMA1; LYSINE; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; RNA POLYMERASE II; STREPTOZOCIN; TRANSCRIPTION FACTOR EZH2; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; COX2 GENE; DIABETIC NEPHROPATHY; EPIGENETICS; GENE; GENE CONTROL; GENE EXPRESSION; HISTONE METHYLATION; IMMUNOBLOTTING; INSULIN DEPENDENT DIABETES MELLITUS; KDM6A GENE; KIDNEY; LAMC1 GENE; MALE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; S100A4 GENE; TRANSCRIPTION REGULATION;

ANIMALS; CHEMOKINE CCL2; CHROMATIN IMMUNOPRECIPITATION; CYCLOOXYGENASE 2; CYCLOPHILINS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETIC NEPHROPATHIES; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HISTONE DEMETHYLASES; KIDNEY; LAMININ; METHYLATION; MICE; RATS; RNA POLYMERASE II; S100 PROTEINS; VIMENTIN;

EID: 84877304423     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2013.47     Document Type: Article

References (52)

1. Brasacchio D, Okabe J, Tikellis C, et al. Hyperglycemia induces a dynamic cooperativity of histone methylase and demethylase enzymes associated with gene-activating epigenetic ks that co-exist on the lysine tail. Diabetes 2009;58:1229-1236.
2. Villeneuve LM, Reddy MA, Lanting LL, et al. Epigenetic histone H3 lysine 9 methylation in metabolic memory and inflammatory phenotype of vascular smooth muscle cells in diabetes. Proc Natl Acad Sci USA 2008;105:9047-9052.
3. Reddy MA, Villeneuve LM, Wang M, et al. Role of the lysine-specific demethylase 1 in the proinflammatory phenotype of vascular smooth muscle cells of diabetic mice. Circ Res 2008;103:615-623.
4. Liu Y, Dentin R, Chen D, et al. A fasting inducible switch modulates gluconeogenesis via activator/coactivator exchange. Nature 2008;456: 269-273.
5. El-Osta A, Brasacchio D, Yao D, et al. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med 2008;205:2409-2417.
6. Miao F, Wu X, Zhang L, et al. Histone methylation patterns are celltype specific in human monocytes and lymphocytes and well maintained at core genes. J Immunol 2008;180:2264-2269.
7. Miao F, Gonzalo IG, Lanting L, et al. In vivo chromatin remodeling events leading to inflammatory gene transcription under diabetic conditions. J Biol Chem 2004;279:18091-18097.
8. Lee HB, Noh H, Seo JY, et al. Histone deacetylase inhibitors: a el class of therapeutic agents in diabetic nephropathy. Kidney Int Suppl 2007; 106:S61-S66.
9. Tikoo K, Meena RL, Kabra DG, et al. Change in post-translational modifications of histone H3, heat-shock protein-27 and MAP kinase p38 expression by curcumin in streptozotocin-induced type I diabetic nephropathy. Br J Pharmacol 2008;153:1225-1231.
10. Miao F, Natara R. Mapping global histone methylation patterns in the coding regions of human genes. Mol Cell Biol 2005;25:4650-4661.
11. Miao F, Wu X, Zhang L, et al. Genome-wide analysis of histone lysine methylation variations caused by diabetic conditions in human monocytes. J Biol Chem 2007;282:13854-13863.
12. Sun G, Reddy MA, Yuan H, et al. Epigenetic histone methylation modulates fibrotic gene expression. J Am Soc Nephrol 2010;21: 2069-2080.
13. Zheng S, Noonan WT, Metreveli NS, et al. Development of late-stage diabetic nephropathy in OVE26 diabetic mice. Diabetes 2004;53: 3248-3257.
14. Naito M, Zager RA, Bomsztyk K. BRG1 increases transcription of proinflammatory genes in renal ischemia. J Am Soc Nephrol 2009; 20:1787-1796.
15. Nelson JD, Flanagin S, Kawata Y, et al. Transcription of laminin g1 chain gene in rat mesangial cells: constitutive and inducible RNA polymerase II recruitment and chromatin states. Am J Physiol Renal Physiol 2008;294:F525-F533.
16. Komers R, Oyama TT, Beard DR, et al. Rho kinase inhibition protects kidneys from diabetic nephropathy without reducing blood pressure. Kidney Int 2011;79:432-442.
17. Komers R, Lindsley JN, Oyama TT, et al. Cyclo-oxygenase-2 inhibition attenuates the progression of nephropathy in uninephrectomized diabetic rats. Clin Exp Pharmacol Physiol 2007;34:36-41.
18. Komers R, Lindsley JN, Oyama TT, et al. Immunohistochemical and functional correlations of renal cyclooxygenase-2 in experimental diabetes. J Clin Invest 2001;107:889-898.
19. Wang J-L, Cheng H-F, Shappell S, et al. Cyclooxygenase-2 (COX-2) inhibition reases proteinuria in a hypertensive diabetic model. J Amer Soc Nephrol 1999;10:A3505.
20. Tesch GH. MCP-1/CCL2: a new diagnostic ker and therapeutic target for progressive renal injury in diabetic nephropathy. Am J Physiol Renal Physiol 2008;294:F697-F701.
21. Rossini M, Cheunsuchon B, Donnert E, et al. Immunolocalization of fibroblast growth factor-1 (FGF-1), its receptor (FGFR-1), and fibroblast-specific protein-1 (FSP-1) in inflammatory renal disease. Kidney Int 2005;68:2621-2628.
22. Coimbra TM, Ssen U, Grone HJ, et al. Early events leading to renal injury in obese Zucker (fatty) rats with type II diabetes. Kidney Int 2000;57:167-182.
23. Setty S, Michael AA, Fish AJ, et al. Differential expression of laminin isoforms in diabetic nephropathy and other renal diseases. Mod Pathol 2012;25:859-868.
24. Eid AA, Ford BM, Block K, et al. AMPK negatively regulates NOX4-dependent activation of p53 and epithelial cell apoptosis in diabetes. J Biol Chem 2010;285:37503-37512.
25. Xu J, Huang Y, Li F, et al. FVB mouse genotype confers susceptibility to OVE26 diabetic albuminuria. Am J Physiol Renal Physiol 2010;299: F487-F494.
26. Nelson JD, Denisenko O, Sova P, et al. Fast chromatin immunoprecipitation assay. Nucleic Acids Res. 2006;34:e2.
27. Flanagin S, Nelson JD, Castner DG, et al. Microplate-based chromatin immunoprecipitation method, Matrix ChIP: a platform to study signaling of complex genomic events. Nucleic Acids Res 2008;36:e17.
28. Nelson JD, Leboeuf RC, Bomsztyk K. Direct recruitment of insulin receptor and ERK signaling cascade to insulin-inducible gene loci. Diabetes 2011;60:127-137.
29. Komers R, Schutzer WE, Reed JF, et al. Altered endothelial nitric oxide synthase targeting and conformation and caveolin-1 expression in the diabetic kidney. Diabetes 2006;55:1651-1659.
30. Cheng HF, Wang CJ, Moeckel GW, et al. Cyclooxygenase-2 inhibitor blocks expression of mediators of renal injury in a model of diabetes and hypertension. Kidney Int 2002;62:929-939.
31. Giunti S, Tesch GH, Pinach S, et al. Monocyte chemoattractant protein-1 has prosclerotic effects both in a mouse model of experimental diabetes and in vitro in human mesangial cells. Diabetologia 2008; 51:198-207.
32. Hargreaves DC, Horng T, Medzhitov R. Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 2009; 138:129-145.
33. Barski A, Cuddapah S, Cui K, et al. High-resolution profiling of histone methylations in the human genome. Cell 2007;129:823-837.
34. Phillips SL, DeRubertis FR, Craven PA. Regulation of the laminin C1 promoter in cultured mesangial cells. Diabetes 1999;48:2083-2089.
35. Yang CW, Hattori M, Vlassara H, et al. Overexpression of transforming growth factor-beta 1 mRNA is associated with up-regulation of glomerular tenascin and laminin gene expression in nonobese diabetic mice. J Am Soc Nephrol 1995;5:1610-1617.
36. Schmid H, Cohen CD, Henger A, et al. Validation of endogenous controls for gene expression analysis in microdissected human renal biopsies. Kidney Int 2003;64:356-360.
37. Swigut T, Wysocka J. H3K27 demethylases, at long last. Cell 2007; 131:29-32.
38. De Santa F, Totaro MG, Prosperini E, et al. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycombmediated gene silencing. Cell 2007;130:1083-1094.
39. Allis CD, Berger SL, Cote J, et al. New nomenclature for chromatinmodifying enzymes. Cell 2007;131:633-636.
40. Villeneuve LM, Reddy MA, Natarajan R. Epigenetics: iphering its role in diabetes and its chronic complications. Clin Exp Pharmacol Physiol 2011;38:401-409.
41. Sayyed SG, Gaikwad AB, Lichtnekert J, et al. Progressive glomerulosclerosis in type 2 diabetes is associated with renal histone H3K9 and H3K23 acetylation, H3K4 dimethylation and phosphorylation at serine 10. Nephrol Dial Transplant 2010;25:1811-1817.
42. Cao R, Wang L, Wang H, et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002;298:1039-1043.
43. Naito M, Shenoy A, Aoyama I, et al. High ambient glucose ments angiotensin ii-induced proinflammatory gene mRNA expression in human mesangial cells: effects of valsartan and simvastatin. Am J Nephrol 2009;30:99-111.
44. Okabe J, Orlowski C, Balcerczyk A, et al. Distinguishing hyperglycemic changes by Set7 in vascular endothelial cells. Circ Res 2012;110: 1067-1076.
45. Gupta J, Tikoo K. Involvement of insulin-induced reversible chromatin remodeling in altering the expression of oxidative stress-responsive genes under hyperglycemia in 3T3-L1 preadipocytes. Gene 2012;504: 181-191.
46. Villeneuve LM, Kato M, Reddy MA, et al. Enhanced levels of microRNA-125b in vascular smooth muscle cells of diabetic db/db mice lead to increased inflammatory gene expression by targeting the histone methyltransferase Suv39h1. Diabetes 2010;59:2904-2915.
47. Nelson J, Denisenko O, Bomsztyk K. Profiling RNA polymerase II using the fast chromatin immunoprecipitation method. Methods Mol Biol 2011;703:219-234.
48. Shanmugam N, Reddy MA, Natarajan R. Distinct roles of heterogeneous nuclear ribonuclear protein K and microRNA-16 in cyclooxygenase-2 RNA stability induced by S100b, a ligand of the receptor for advanced glycation end products. J Biol Chem 2008;283:36221-36233.
49. Wang B, Komers R, Carew R, et al. Suppression of microRNA-29 expression by TGF-beta1 promotes collagen expression and renal fibrosis. J Am Soc Nephrol 2012;23:252-265.
50. Li Y, Reddy MA, Miao F, et al. Role of the histone H3 lysine 4 methyltransferase, SET7/9, in the regulation of NF-kappaB-dependent inflammatory genes. Relevance to diabetes and inflammation. J Biol Chem 2008;283:26771- 26781.
51. Naito M, Bomsztyk K, Zager RA. Renal ischemia-induced cholesterol loading: transcription factor recruitment and chromatin remodeling along the HMG CoA reductase gene. Am J Pathol 2009; 174:54-62.
52. Euskirchen GM, Rozowsky JS, Wei CL, et al. Mapping of transcription factor binding regions in mammalian cells by ChIP: comparison of arrayand sequencing-based technologies. Genome Res 2007;17:898-909.