Table of Contents Author Guidelines Submit a Manuscript
Journal of Diabetes Research
Volume 2017, Article ID 7242384, 11 pages
https://doi.org/10.1155/2017/7242384
Review Article

Role of Epigenetic Histone Modifications in Diabetic Kidney Disease Involving Renal Fibrosis

Department of Nephrology, Second Hospital of Jilin University, Changchun 130041, China

Correspondence should be addressed to Lining Miao; moc.361@55gniniloaim

Received 22 December 2016; Accepted 14 March 2017; Published 13 June 2017

Academic Editor: Wei J. Liu

Copyright © 2017 Jing Sun et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Y. S. Kanwar, L. Sun, P. Xie, F. Y. Liu, and S. Chen, “A glimpse of various pathogenetic mechanisms of diabetic nephropathy,” Annual Review of Pathology, vol. 6, pp. 395–423, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. F. P. Schena and L. Gesualdo, “Pathogenetic mechanisms of diabetic nephropathy,” Journal of the American Society of Nephrology, vol. 16, Supplement 1, pp. S30–S33, 2005. View at Google Scholar
  3. G. Wolf, “New insights into the pathophysiology of diabetic nephropathy: from haemodynamics to molecular pathology,” European Journal of Clinical Investigation, vol. 34, no. 12, pp. 785–796, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. C. R. Ban and S. M. Twigg, “Fibrosis in diabetes complications: pathogenic mechanisms and circulating and urinary markers,” Vascular Health and Risk Management, vol. 4, no. 3, pp. 575–596, 2008. View at Google Scholar
  5. L. M. Villeneuve, M. A. Reddy, and R. Natarajan, “Epigenetics: deciphering its role in diabetes and its chronic complications,” Clinical and Experimental Pharmacology & Physiology, vol. 38, no. 7, pp. 451–459, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. L. M. Villeneuve and R. Natarajan, “Epigenetic mechanisms,” Contributions to Nephrology, vol. 170, pp. 57–65, 2011. View at Google Scholar
  7. C. Hu, L. Sun, L. Xiao et al., “Insights into the mechanisms involved in the expression and regulation of extracellular matrix proteins in diabetic nephropathy,” Current Medicinal Chemistry, vol. 22, no. 24, pp. 2858–2870, 2015. View at Publisher · View at Google Scholar
  8. E. C. Tsilibary, “Microvascular basement membranes in diabetes mellitus,” The Journal of Pathology, vol. 200, no. 4, pp. 537–546, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. Y. Liu, Z. Wang, W. Yin et al., “Severe insulin resistance and moderate glomerulosclerosis in a minipig model induced by high-fat/ high-sucrose/ high-cholesterol diet,” Experimental Animals, vol. 56, no. 1, pp. 11–20, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. B. Olgemoller and E. Schleicher, “Alterations of glomerular matrix proteins in the pathogenesis of diabetic nephropathy,” The Clinical Investigator, vol. 71, 5 Supplement, pp. S13–S19, 1993. View at Google Scholar
  11. M. B. Stokes, S. Holler, Y. Cui et al., “Expression of decorin, biglycan, and collagen type I in human renal fibrosing disease,” Kidney International, vol. 57, no. 2, pp. 487–498, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. L. Schaefer, I. Raslik, H. J. Grone et al., “Small proteoglycans in human diabetic nephropathy: discrepancy between glomerular expression and protein accumulation of decorin, biglycan, lumican, and fibromodulin,” The FASEB Journal, vol. 15, no. 3, pp. 559–561, 2001. View at Publisher · View at Google Scholar
  13. A. Matheson, M. D. Willcox, J. Flanagan, and B. J. Walsh, “Urinary biomarkers involved in type 2 diabetes: a review,” Diabetes/Metabolism Research and Reviews, vol. 26, no. 3, pp. 150–171, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Tashiro, I. Koyanagi, I. Ohara et al., “Levels of urinary matrix metalloproteinase-9 (MMP-9) and renal injuries in patients with type 2 diabetic nephropathy,” Journal of Clinical Laboratory Analysis, vol. 18, no. 3, pp. 206–210, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Granier, K. Makni, L. Molina, B. Jardin-Watelet, H. Ayadi, and F. Jarraya, “Gene and protein markers of diabetic nephropathy,” Nephrology, Dialysis, Transplantation, vol. 23, no. 3, pp. 792–799, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. C. E. Hills, R. Bland, J. Bennett, P. M. Ronco, and P. E. Squires, “TGF-beta1 mediates glucose-evoked up-regulation of connexin-43 cell-to-cell communication in HCD-cells,” Cellular Physiology and Biochemistry, vol. 24, no. 3-4, pp. 177–186, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. E. P. Bottinger and M. Bitzer, “TGF-beta signaling in renal disease,” Journal of the American Society of Nephrology, vol. 13, no. 10, pp. 2600–2610, 2002. View at Google Scholar
  18. C. E. Hills and P. E. Squires, “TGF-beta1-induced epithelial-to-mesenchymal transition and therapeutic intervention in diabetic nephropathy,” American Journal of Nephrology, vol. 31, no. 1, pp. 68–74, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. J. M. Veeneman, P. E. de Jong, R. M. Huisman, and D. J. Reijngoud, “Re: Adey et al. Reduced synthesis of muscle proteins in chronic renal failure. Am J Physiol Endocrinol Metab 278: E219-E225, 2000,” American Journal of Physiology. Endocrinology and Metabolism, vol. 280, no. 1, pp. E197–E198, 2001. View at Google Scholar
  20. K. Sharma, F. N. Ziyadeh, B. Alzahabi et al., “Increased renal production of transforming growth factor-beta1 in patients with type II diabetes,” Diabetes, vol. 46, no. 5, pp. 854–859, 1997. View at Publisher · View at Google Scholar
  21. H. S. Lee, “Pathogenic role of TGF-beta in the progression of podocyte diseases,” Histology and Histopathology, vol. 26, no. 1, pp. 107–116, 2011. View at Publisher · View at Google Scholar
  22. H. S. Lee and C. Y. Song, “Differential role of mesangial cells and podocytes in TGF-beta-induced mesangial matrix synthesis in chronic glomerular disease,” Histology and Histopathology, vol. 24, no. 7, pp. 901–908, 2009. View at Publisher · View at Google Scholar
  23. C. Dai and Y. Liu, “Hepatocyte growth factor antagonizes the profibrotic action of TGF-beta1 in mesangial cells by stabilizing Smad transcriptional corepressor TGIF,” Journal of the American Society of Nephrology, vol. 15, no. 6, pp. 1402–1412, 2004. View at Google Scholar
  24. C. E. Hills, N. Al-Rasheed, N. Al-Rasheed, G. B. Willars, and N. J. Brunskill, “C-peptide reverses TGF-beta1-induced changes in renal proximal tubular cells: implications for treatment of diabetic nephropathy,” American Journal of Physiology. Renal Physiology, vol. 296, no. 3, pp. F614–F621, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. C. Tikellis, M. E. Cooper, S. M. Twigg, W. C. Burns, and M. Tolcos, “Connective tissue growth factor is up-regulated in the diabetic retina: amelioration by angiotensin-converting enzyme inhibition,” Endocrinology, vol. 145, no. 2, pp. 860–866, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. P. Roestenberg, F. A. van Nieuwenhoven, J. A. Joles et al., “Temporal expression profile and distribution pattern indicate a role of connective tissue growth factor (CTGF/CCN-2) in diabetic nephropathy in mice,” American Journal of Physiology. Renal Physiology, vol. 290, no. 6, pp. F1344–F1354, 2006. View at Google Scholar
  27. T. Umezono, M. Toyoda, M. Kato et al., “Glomerular expression of CTGF, TGF-beta 1 and type IV collagen in diabetic nephropathy,” Journal of Nephrology, vol. 19, no. 6, pp. 751–757, 2006. View at Google Scholar
  28. B. S. Weston, N. A. Wahab, and R. M. Mason, “CTGF mediates TGF-beta-induced fibronectin matrix deposition by upregulating active alpha5beta1 integrin in human mesangial cells,” Journal of the American Society of Nephrology, vol. 14, no. 3, pp. 601–610, 2003. View at Google Scholar
  29. H. M. Kok, L. L. Falke, R. Goldschmeding, and T. Q. Nguyen, “Targeting CTGF, EGF and PDGF pathways to prevent progression of kidney disease,” Nature Reviews. Nephrology, vol. 10, no. 12, pp. 700–711, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. D. Tampe and M. Zeisberg, “Potential approaches to reverse or repair renal fibrosis,” Nature Reviews. Nephrology, vol. 10, no. 4, pp. 226–237, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. I. Loeffler and G. Wolf, “Epithelial-to-mesenchymal transition in diabetic nephropathy: fact or fiction?” Cell, vol. 4, no. 4, pp. 631–652, 2015. View at Publisher · View at Google Scholar
  32. P. Galichon and A. Hertig, “Epithelial to mesenchymal transition as a biomarker in renal fibrosis: are we ready for the bedside?” Fibrogenesis Tissue Repair, vol. 4, 11 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Fragiadaki and R. M. Mason, “Epithelial-mesenchymal transition in renal fibrosis - evidence for and against,” International Journal of Experimental Pathology, vol. 92, no. 3, pp. 143–150, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Zeisberg, J. Hanai, H. Sugimoto et al., “BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury,” Nature Medicine, vol. 9, no. 7, pp. 964–968, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. W. T. D. E. R. Group, “Effect of intensive therapy on the microvascular complications of type 1 diabetes mellitus,” Jama, vol. 287, no. 19, pp. 2563–2569, 2002. View at Publisher · View at Google Scholar
  36. Writing Team for the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group, “Sustained effect of intensive treatment of type 1 diabetes mellitus on development and progression of diabetic nephropathy: the Epidemiology of Diabetes Interventions and Complications (EDIC) study,” Jama, vol. 290, no. 16, pp. 2159–2167, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. G. Schernthaner, “Diabetes and cardiovascular disease: is intensive glucose control beneficial or deadly? Lessons from ACCORD, ADVANCE, VADT, UKPDS, PROactive, and NICE-SUGAR,” Wiener Medizinische Wochenschrift (1946), vol. 160, no. 1-2, pp. 8–19, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. S. L. Li, M. A. Reddy, Q. Cai et al., “Enhanced proatherogenic responses in macrophages and vascular smooth muscle cells derived from diabetic db/db mice,” Diabetes, vol. 55, no. 9, pp. 2611–2619, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. R. A. Kowluru, S. N. Abbas, and S. Odenbach, “Reversal of hyperglycemia and diabetic nephropathy: effect of reinstitution of good metabolic control on oxidative stress in the kidney of diabetic rats,” Journal of Diabetes and Its Complications, vol. 18, no. 5, pp. 282–288, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. H. P. Hammes, I. Klinzing, S. Wiegand, R. G. Bretzel, A. M. Cohen, and K. Federlin, “Islet transplantation inhibits diabetic retinopathy in the sucrose-fed diabetic Cohen rat,” Investigative Ophthalmology & Visual Science, vol. 34, no. 6, pp. 2092–2096, 1993. View at Google Scholar
  41. C. H. Waddington, “The epigenotype. 1942,” International Journal of Epidemiology, vol. 41, no. 1, pp. 10–13, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. P. W. Franks and J. A. Nettleton, “Invited commentary: gene X lifestyle interactions and complex disease traits—inferring cause and effect from observational data, sine qua non,” American Journal of Epidemiology, vol. 172, no. 9, pp. 992–997, 2010, discussion 998-999. View at Publisher · View at Google Scholar · View at Scopus
  43. M. R. Wing, A. Ramezani, H. S. Gill, J. M. Devaney, and D. S. Raj, “Epigenetics of progression of chronic kidney disease: fact or fantasy?” Seminars in Nephrology, vol. 33, no. 4, pp. 363–374, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. M. A. Reddy, J. Tak Park, and R. Natarajan, “Epigenetic modifications in the pathogenesis of diabetic nephropathy,” Seminars in Nephrology, vol. 33, no. 4, pp. 341–353, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. T. Kouzarides, “Chromatin modifications and their function,” Cell, vol. 128, no. 4, pp. 693–705, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. R. Bonasio, S. Tu, and D. Reinberg, “Molecular signals of epigenetic states,” Science, vol. 330, no. 6004, pp. 612–616, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. V. W. Zhou, A. Goren, and B. E. Bernstein, “Charting histone modifications and the functional organization of mammalian genomes,” Nature Reviews. Genetics, vol. 12, no. 1, pp. 7–18, 2011. View at Google Scholar
  48. L. M. Villeneuve and R. Natarajan, “The role of epigenetics in the pathology of diabetic complications,” American Journal of Physiology. Renal Physiology, vol. 299, no. 1, pp. F14–F25, 2010. View at Google Scholar
  49. R. Murr, “Interplay between different epigenetic modifications and mechanisms,” Advances in Genetics, vol. 70, pp. 101–141, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. M. A. Reddy and R. Natarajan, “Epigenetics in diabetic kidney disease,” Journal of the American Society of Nephrology, vol. 22, no. 12, pp. 2182–2185, 2011. View at Google Scholar
  51. X. J. Yang and E. Seto, “HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention,” Oncogene, vol. 26, no. 37, pp. 5310–5318, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. A. J. de Ruijter, A. H. van Gennip, H. N. Caron, S. Kemp, and A. B. van Kuilenburg, “Histone deacetylases (HDACs): characterization of the classical HDAC family,” The Biochemical Journal, vol. 370, Part 3, pp. 737–749, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Jorgensen, G. Schotta, and C. S. Sorensen, “Histone H4 lysine 20 methylation: key player in epigenetic regulation of genomic integrity,” Nucleic Acids Research, vol. 41, no. 5, pp. 2797–2806, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. G. D. Sun, W. P. Cui, Q. Y. Guo, and L. N. Miao, “Histone lysine methylation in diabetic nephropathy,” Journal of Diabetes Research, vol. 2014, Article ID 654148, 9 pages, 2014. View at Google Scholar
  55. M. Wegner, D. Neddermann, M. Piorunska-Stolzmann, and P. P. Jagodzinski, “Role of epigenetic mechanisms in the development of chronic complications of diabetes,” Diabetes Research and Clinical Practice, vol. 105, no. 2, pp. 164–175, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Tonna, A. El-Osta, M. E. Cooper, and C. Tikellis, “Metabolic memory and diabetic nephropathy: potential role for epigenetic mechanisms,” Nature Reviews. Nephrology, vol. 6, no. 6, pp. 332–341, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. M. C. Thomas, “Epigenetic mechanisms in diabetic kidney disease,” Current Diabetes Reports, vol. 16, no. 3, p. 31, 2016. View at Google Scholar
  58. C. Ling and L. Groop, “Epigenetics: a molecular link between environmental factors and type 2 diabetes,” Diabetes, vol. 58, no. 12, pp. 2718–2725, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. S. K. Chakrabarti, J. Francis, S. M. Ziesmann, J. C. Garmey, and R. G. Mirmira, “Covalent histone modifications underlie the developmental regulation of insulin gene transcription in pancreatic beta cells,” The Journal of Biological Chemistry, vol. 278, no. 26, pp. 23617–23623, 2003. View at Publisher · View at Google Scholar · View at Scopus
  60. M. A. Reddy and R. Natarajan, “Epigenetic mechanisms in diabetic vascular complications,” Cardiovascular Research, vol. 90, no. 3, pp. 421–429, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. F. Miao, I. G. Gonzalo, L. Lanting, and R. Natarajan, “In vivo chromatin remodeling events leading to inflammatory gene transcription under diabetic conditions,” The Journal of Biological Chemistry, vol. 279, no. 17, pp. 18091–18097, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. H. Yuan, M. A. Reddy, G. Sun et al., “Involvement of p300/CBP and epigenetic histone acetylation in TGF-beta1-mediated gene transcription in mesangial cells,” American Journal of Physiology. Renal Physiology, vol. 304, no. 5, pp. F601–F613, 2013. View at Google Scholar
  63. G. Sun, M. A. Reddy, H. Yuan, L. Lanting, M. Kato, and R. Natarajan, “Epigenetic histone methylation modulates fibrotic gene expression,” Journal of the American Society of Nephrology, vol. 21, no. 12, pp. 2069–2080, 2010. View at Google Scholar
  64. Y. Wang, Y. Wang, M. Luo et al., “Novel curcumin analog C66 prevents diabetic nephropathy via JNK pathway with the involvement of p300/CBP-mediated histone acetylation,” Biochimica et Biophysica Acta, vol. 1852, no. 1, pp. 34–46, 2015. View at Google Scholar
  65. S. O. Kolset, F. P. Reinholt, and T. Jenssen, “Diabetic nephropathy and extracellular matrix,” The Journal of Histochemistry and Cytochemistry, vol. 60, no. 12, pp. 976–986, 2012. View at Publisher · View at Google Scholar · View at Scopus
  66. F. C. Brosius 3rd, “New insights into the mechanisms of fibrosis and sclerosis in diabetic nephropathy,” Reviews in Endocrine & Metabolic Disorders, vol. 9, no. 4, pp. 245–254, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. M. K. Diamond-Stanic, Y. H. You, and K. Sharma, “Sugar, sex, and TGF-beta in diabetic nephropathy,” Seminars in Nephrology, vol. 32, no. 3, pp. 261–268, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. A. K. Ghosh, S. Bhattacharyya, R. Lafyatis et al., “p300 is elevated in systemic sclerosis and its expression is positively regulated by TGF-beta: epigenetic feed-forward amplification of fibrosis,” The Journal of Investigative Dermatology, vol. 133, no. 5, pp. 1302–1310, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. Y. Kanamaru, A. Nakao, Y. Tanaka et al., “Involvement of p300 in TGF-beta/Smad-pathway-mediated alpha2(I) collagen expression in mouse mesangial cells,” Nephron. Experimental Nephrology, vol. 95, no. 1, pp. e36–e42, 2003. View at Publisher · View at Google Scholar
  70. M. Fang, X. Kong, P. Li et al., “RFXB and its splice variant RFXBSV mediate the antagonism between IFNgamma and TGFbeta on COL1A2 transcription in vascular smooth muscle cells,” Nucleic Acids Research, vol. 37, no. 13, pp. 4393–4406, 2009. View at Publisher · View at Google Scholar · View at Scopus
  71. H. Xu, X. Wu, H. Qin et al., “Myocardin-related transcription factor a epigenetically regulates renal fibrosis in diabetic nephropathy,” Journal of the American Society of Nephrology, vol. 26, no. 7, pp. 1648–1660, 2015. View at Google Scholar
  72. H. Yuan, M. A. Reddy, S. Deshpande et al., “Epigenetic histone modifications involved in profibrotic gene regulation by 12/15-lipoxygenase and its oxidized lipid products in diabetic nephropathy,” Antioxidants & Redox Signaling, vol. 24, no. 7, pp. 361–375, 2016. View at Publisher · View at Google Scholar · View at Scopus
  73. H. B. Lee, H. Noh, J. Y. Seo, M. R. Yu, and H. Ha, “Histone deacetylase inhibitors: a novel class of therapeutic agents in diabetic nephropathy,” Kidney International. Supplement, vol. 73, no. 106, pp. S61–S66, 2007. View at Google Scholar
  74. X. Wang, J. Liu, J. Zhen et al., “Histone deacetylase 4 selectively contributes to podocyte injury in diabetic nephropathy,” Kidney International, vol. 86, no. 4, pp. 712–725, 2014. View at Publisher · View at Google Scholar · View at Scopus
  75. M. Yoshikawa, K. Hishikawa, T. Marumo, and T. Fujita, “Inhibition of histone deacetylase activity suppresses epithelial-to-mesenchymal transition induced by TGF-beta1 in human renal epithelial cells,” Journal of the American Society of Nephrology, vol. 18, no. 1, pp. 58–65, 2007. View at Google Scholar
  76. M. Pang, J. Kothapally, H. Mao et al., “Inhibition of histone deacetylase activity attenuates renal fibroblast activation and interstitial fibrosis in obstructive nephropathy,” American Journal of Physiology. Renal Physiology, vol. 297, no. 4, pp. F996–F1005, 2009. View at Google Scholar
  77. H. Noh, E. Y. Oh, J. Y. Seo et al., “Histone deacetylase-2 is a key regulator of diabetes- and transforming growth factor-beta1-induced renal injury,” American Journal of Physiology. Renal Physiology, vol. 297, no. 3, pp. F729–F739, 2009. View at Google Scholar
  78. N. Liu, S. He, L. Ma et al., “Blocking the class I histone deacetylase ameliorates renal fibrosis and inhibits renal fibroblast activation via modulating TGF-beta and EGFR signaling,” PloS One, vol. 8, no. 1, article e54001, 2013. View at Publisher · View at Google Scholar · View at Scopus
  79. O. G. McDonald, H. Wu, W. Timp, A. Doi, and A. P. Feinberg, “Genome-scale epigenetic reprogramming during epithelial-to-mesenchymal transition,” Nature Structural & Molecular Biology, vol. 18, no. 8, pp. 867–874, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. S. Chen, B. Feng, B. George, R. Chakrabarti, M. Chen, and S. Chakrabarti, “Transcriptional coactivator p300 regulates glucose-induced gene expression in endothelial cells,” American Journal of Physiology. Endocrinology and Metabolism, vol. 298, no. 1, pp. E127–E137, 2010. View at Google Scholar
  81. J. M. Yun, I. Jialal, and S. Devaraj, “Epigenetic regulation of high glucose-induced proinflammatory cytokine production in monocytes by curcumin,” The Journal of Nutritional Biochemistry, vol. 22, no. 5, pp. 450–458, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. J. Ma, L. Phillips, Y. Wang et al., “Curcumin activates the p38MPAK-HSP25 pathway in vitro but fails to attenuate diabetic nephropathy in DBA2J mice despite urinary clearance documented by HPLC,” BMC Complementary and Alternative Medicine, vol. 10, p. 67, 2010. View at Google Scholar
  83. S. Khan, G. Jena, and K. Tikoo, “Sodium valproate ameliorates diabetes-induced fibrosis and renal damage by the inhibition of histone deacetylases in diabetic rat,” Experimental and Molecular Pathology, vol. 98, no. 2, pp. 230–239, 2015. View at Publisher · View at Google Scholar · View at Scopus
  84. H. Qi, Z. Jing, W. Xiaolin et al., “Histone demethylase JMJD2A inhibition attenuates neointimal hyperplasia in the carotid arteries of balloon-injured diabetic rats via transcriptional silencing: inflammatory gene expression in vascular smooth muscle cells,” Cellular Physiology and Biochemistry, vol. 37, no. 2, pp. 719–734, 2015. View at Publisher · View at Google Scholar · View at Scopus
  85. R. E. Gilbert, Q. Huang, K. Thai et al., “Histone deacetylase inhibition attenuates diabetes-associated kidney growth: potential role for epigenetic modification of the epidermal growth factor receptor,” Kidney International, vol. 79, no. 12, pp. 1312–1321, 2011. View at Publisher · View at Google Scholar · View at Scopus
  86. A. Advani, Q. Huang, K. Thai et al., “Long-term administration of the histone deacetylase inhibitor vorinostat attenuates renal injury in experimental diabetes through an endothelial nitric oxide synthase-dependent mechanism,” The American Journal of Pathology, vol. 178, no. 5, pp. 2205–2214, 2011. View at Publisher · View at Google Scholar · View at Scopus
  87. S. Khan and G. Jena, “Sodium butyrate, a HDAC inhibitor ameliorates eNOS, iNOS and TGF-beta1-induced fibrogenesis, apoptosis and DNA damage in the kidney of juvenile diabetic rats,” Food and Chemical Toxicology, vol. 73, pp. 127–139, 2014. View at Publisher · View at Google Scholar · View at Scopus