The advances of epigenetics in diabetic retinopathy_Chinese Journal of Ocular Fundus Diseases

Authors：

Li Zhongting ,  Leng Xuan , Zhao Qi

Department of Ophthalmology, Zhongshan City People's Hospital, Zhongshan 528403, China;

Corresponding author：

Leng Xuan, Email: 584593304@qq.com

Keywords：

Diabetic retinopathy/genetics; Epigenesis, genetic; Review

DOI：

10.3760/cma.j.issn.1005-1015.2019.02.018

Video：

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Epigenetics refers to the changes in gene expression level and function caused by non-genetic sequence changes. It can provide the time, location and mode of the genetic information for the execution of DNA sequences, including DNA methylation, histone modification, non-coding RNA and chromatin remodeling. Studies had shown that epigenetics plays an important role in the development of diabetic retinopathy (DR), and it had been found that epigenetic-related treatment regimens had a certain effect on the treatment of DR through animal experiments and in vitro experiments. It was benefit to regulate the development of diabetes and its complications by depth study of DNA methylation, histone modification, miRNA and metabolic memory. An understanding of changes in gene transcriptional mechanisms at the epigenetic level could help us to further study the prevention and control of diabetes and its complications, and to provide new ideas for treatment.

Citation： Li Zhongting, Leng Xuan, Zhao Qi. The advances of epigenetics in diabetic retinopathy. Chinese Journal of Ocular Fundus Diseases, 2019, 35(2): 196-199. doi: 10.3760/cma.j.issn.1005-1015.2019.02.018 Copy

1.	Abhary S, Hewitt AW, Burdon KP, et al. A systematic meta-analysis of genetic association studies for diabetic retinopathy[J]. Diabetes, 2009, 58(9): 2137-2147. DOI: 10.2337/db09-0059.
2.	Waddington CH. The epigenotype 1942[J]. Int J Epidemiol, 2012, 41(1): 10-13. DOI: 10.1093/ije/dyr184.
3.	Portela A, Esteller M. Epigenetic modifications and human disease[J]. Nat Biotechnol, 2010, 28(10): 1057-1068. DOI: 10.1038/nbt.1685.
4.	Perrone L, Devi TS, Hosoya K, et al. Thioredoxin interacting protein (TXNIP) induces inflammation through chromatin modification in retinal capillary endothelial cells under diabetic conditions[J]. J Cell Physiol, 2009, 221(1): 262-272. DOI: 10.1002/jcp.21852.
5.	Kadiyala CS, Zheng L, Du Y, et al. Acetylation of retinal histones in diabetes increases inflammatory proteins: effects of minocycline and manipulation of histone acetyltransferase (HAT) and histone deacetylase (HDAC)[J]. J Biol Chem, 2012, 287(31): 25869-25880. DOI: 10.1074/jbc.M112.375204.
6.	Herencia-Bueno KE, Aldrovani M, Crivelaro RM, et al. Reduction in histone H3 acetylation and chromatin remodeling in corneas of alloxan-induced diabetic rats[J]. Cornea, 2018, 37(5): 624-632. DOI: 10.1097/ICO.0000000000001533.
7.	Wu JH, Gao Y, Ren AJ, et al. Altered microRNA expression profiles in retinas with diabetic retinopathy[J]. Ophthalmic Res, 2012, 47(4): 195-201. DOI: 10.1159/000331992.
8.	Radović N, Nikolić Jakoba N, Petrović N, et al. MicroRNA-146a and microRNA-155 as novel crevicular fluid biomarkers for periodontitis in non-diabetic and type 2 diabetic patients[J]. J Clin Periodontol, 2018, 45(6): 663-671. DOI: 10.1111/jcpe.12888.
9.	Fan B, Luk AOY, Chan JCN, et al. MicroRNA and diabetic complications: a clinical perspective[J]. Antioxid Redox Signal, 2018, 29(11): 1041-1063. DOI: 10.1089/ars.2017.7318.
10.	Ungerbäck J, Hosokawa H, Wang X, et al. Pioneering, chromatin remodeling, and epigenetic constraint in early T-cell gene regulation by SPI1 (PU.1)[J]. Genome Res, 2018, 28(10): 1508-1519. DOI: 10.1101/gr.231423.117.
11.	Zhong Q, Kowluru RA. Epigenetic changes in mitochondrial superoxide dismutase in the retina and the development of diabetic retinopathy[J]. Diabetes, 2011, 60(4): 1304-1313. DOI: 10.2337/db10-0133.
12.	Miao F, Wu X, Zhang L, et al. Genome-wide analysis of histone lysine methylation variations caused by diabetic conditions in human monocytes[J]. J Biol Chem, 2007, 282(18): 13854-13863. DOI: 10.1074/jbc.M609446200.
13.	Zhong Q, Kowluru RA. Role of histone acetylation in the development of diabetic retinopathy and the metabolic memory phenomenon[J]. J Cell Biochem, 2010, 110(6): 1306-1313. DOI: 10.1002/jcb.22644.
14.	Brasacchio D, Okabe J, Tikellis C, et al. Hyperglycemia induces a dynamic cooperativity of histone methylase and demethylase enzymes associated with gene-activating epigenetic marks that coexist on the lysine tail[J]. Diabetes, 2009, 58(5): 1229-1236. DOI: 10.2337/db08-1666.
15.	Deering TG, Ogihara T, Trace AP, et al. Methyltransferase Set7/9 maintains transcription and euchromatin structure at islet-enriched genes[J]. Diabetes, 2009, 58(1): 185-193. DOI: 10.2337/db08-1150.
16.	Tewari S, Zhong Q, Santos JM, et al. Mitochondria DNA replication and DNA methylation in the metabolic memory associated with continued progression of diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2012, 53(8): 4881-4888. DOI: 10.1167/iovs.12-9732.
17.	Mishra M, Kowluru RA. Epigenetic modification of mitochondrial DNA in the development of diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2015, 56(9): 5133-5142. DOI: 10.1167/iovs.15-16937.
18.	Mishra M, Kowluru RA. The role of DNA methylation in the metabolic memory phenomenon associated with the continued progression of diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2016, 57(13): 5748-5757. DOI: 10.1167/iovs.16-19759.
19.	Kowluru RA, Shan Y, Mishra M. Dynamic DNA methylation of matrix metalloproteinase-9 in the development of diabetic retinopathy[J]. Lab Invest, 2016, 96(10): 1040-1049. DOI: 10.1038/labinvest.2016.78.
20.	Miao F, Gonzalo IG, Lanting L, et al. In vivo chromatin remodeling events leading to inflammatory gene transcription under diabetic conditions[J]. J Biol Chem, 2004, 279(17): 18091-18097. DOI: 10.1074/jbc.M311786200.
21.	Xu B, Chiu J, Feng B, et al. PARP activation and the alteration of vasoactive factors and extracellular matrix protein in retina and kidney in diabetes[J]. Diabetes Metab Res Rev, 2008, 24(5): 404-412. DOI: 10.1002/dmrr.842.
22.	Gao J, Zheng Z, Gu Q, et al. Deacetylation of MnSOD by PARP-regulated SIRT3 protects retinal capillary endothelial cells from hyperglycemia-induced damage[J]. Biochem Biophys Res Commun, 2016, 472(3): 425-431. DOI: 10.1016/j.bbrc.2015.12.037.
23.	Zhong Q, Kowluru RA. Epigenetic modification of Sod2 in the development of diabetic retinopathy and in the metabolic memory: role of histone methylation[J]. Invest Ophthalmol Vis Sci, 2013, 54(1): 244-250. DOI: 10.1167/iovs.12-10854.
24.	Ye P, Liu J, He F, et al. Hypoxia-induced deregulation of miR-126 and its regulative effect on VEGF and MMP-9 expression[J]. Int J Med Sci, 2013, 11(1): 17-23. DOI: 10.7150/ijms.7329.
25.	Li EH, Huang QZ, Li GC, et al. Effects of miRNA-200b on the development of diabetic retinopathy by targeting VEGFA gene[J/OL]. Biosci Rep, 2017, 37(2): BSR20160572[2017-04-30]. http://www.bioscirep.org/cgi/pmidlookup?view=long&pmid=28122882. DOI: 10.1042/BSR20160572.
26.	Kovacs B, Lumayag S, Cowan C, et al. MicroRNAs in early diabetic retinopathy in streptozotocin-induced diabetic rats[J]. Invest Ophthalmol Vis Sci, 2011, 52(7): 4402-4409. DOI: 10.1167/iovs.10-6879.
27.	Ling S, Birnbaum Y, Nanhwan MK, et al. MicroRNA-dependent cross-talk between VEGF and HIF1α in the diabetic retina[J]. Cell Signal, 2013, 25(12): 2840-2847. DOI: 10.1016/j.cellsig.2013.08.039.
28.	Haque R, Hur EH, Farrell AN, et al. MicroRNA-152 represses VEGF and TGFβ1 expressions through post-transcriptional inhibition of (Pro)renin receptor in human retinal endothelial cells[J]. Mol Vis, 2015, 21: 224-235.
29.	Pirola L. The DCCT/EDIC study: epigenetic clues after three decades[J]. Diabetes, 2014, 63(5): 1460-1462. DOI: 10.2337/db14-0238.
30.	Diabetes Control and Complications Trial (DCCT)/Epidemiology of Diabetes Interventions and Complications (EDIC) Research Group, Lachin JM, White NH, et al. Effect of intensive diabetes therapy on the progression of diabetic retinopathy in patients with type 1 diabetes: 18 years of follow-up in the DCCT/EDIC[J]. Diabetes, 2015, 64(2): 631-642. DOI: 10.2337/db14-0930.
31.	Chen Z, Miao F, Paterson AD, et al. Epigenomic profiling reveals an association between persistence of DNA methylation and metabolic memory in the DCCT/EDIC type 1 diabetes cohort[J]. Proc Natl Acad Sci USA, 2016, 113(21): 3002-3011. DOI: 10.1073/pnas.1603712113.
32.	Miao F, Chen Z, Genuth S, et al. Evaluating the role of epigenetic histone modifications in the metabolic memory of type 1 diabetes[J]. Diabetes, 2014, 63(5): 1748-1762. DOI: 10.2337/db13-1251.
33.	Kowluru RA, Chan PS. Metabolic memory in diabetes – from in vitro oddity to in vivo problem: role of apoptosis[J]. Brain Res Bull, 2010, 81(2-3): 297-302. DOI: 10.1016/j.brainresbull.2009.05.006.
34.	Kowluru RA, Kanwar M, Kennedy A. Metabolic memory phenomenon and accumulation of peroxynitrite in retinal capillaries[J]. Exp Diabetes Res, 2007, 2007: 21976. DOI: 10.1155/2007/21976.
35.	Kanwar M, Kowluru RA. Role of glyceraldehyde 3-phosphate dehydrogenase in the development and progression of diabetic retinopathy[J]. Diabetes, 2009, 58(1): 227-234. DOI: 10.2337/db08-1025.
36.	Berthiaume M, Boufaied N, Moisan A, et al. High levels of oxidative stress globally inhibit gene transcription and histone acetylation[J]. DNA Cell Biol, 2006, 25(2): 124-134. DOI: 10.1089/dna.2006.25.124.
37.	Liu W, Cui Y, Ren W, et al. Epigenetic biomarker screening by FLIM-FRET for combination therapy in ER+ breast cancer[J]. Clin Epigenetics, 2019, 11(1): 16. DOI: 10.1186/s13148-019-0620-6.
38.	Duan YT, Yang XA, Fang LY, et al. Anti-proliferative and anti-invasive effects of garcinol from Garcinia indica on gallbladder carcinoma cells[J]. Pharmazie, 2018, 73(7): 413-417. DOI: 10.1691/ph.2018.8366.
39.	Di Martile M, Desideri M, De Luca T, et al. Histone acetyltransferase inhibitor CPTH6 preferentially targets lung cancer stem-like cells[J]. Oncotarget, 2016, 7(10): 11332-11348. DOI: 10.18632/oncotarget.7238.
40.	Yang Y, Liu K, Liang Y, et al. Histone acetyltransferase inhibitor C646 reverses epithelial to mesenchymal transition of human peritoneal mesothelial cells via blocking TGF-β1/Smad3 signaling pathway in vitro[J]. Int J Clin Exp Pathol, 2015, 8(3): 2746-2754.
41.	Gao Y, Zhang C, Chang J, et al. Enzyme-instructed self-assembly of a novel histone deacetylase inhibitor with enhanced selectivity and anticancer efficiency[J/OL]. Biomater Sci, 2019, 2019: E1[2019-01-23]. https://doi.org/10.1039/c8bm01422a. DOI: 10.1039/c8bm01422a. [published online ahead of print].
42.	Takai N, Ueda T, Nishida M, et al. A novel histone deacetylase inhibitor, Scriptaid, induces growth inhibition, cell cycle arrest and apoptosis in human endometrial cancer and ovarian cancer cells[J]. Int J Mol Med, 2006, 17(2): 323-329.
43.	Hakami NY, Dusting GJ, Peshavariya HM. Trichostatin A, a histone deacetylase inhibitor suppresses NADPH oxidase 4-derived redox signalling and angiogenesis[J]. J Cell Mol Med, 2016, 20(10): 1932-1944. DOI: 10.1111/jcmm.12885.
44.	Crosson CE, Mani SK, Husain S, et al. Inhibition of histone deacetylase protects the retina from ischemic injury[J]. Invest Ophthalmol Vis Sci, 2010, 51(7): 3639-3645. DOI: 10.1111/jcmm.12885.

1. Abhary S, Hewitt AW, Burdon KP, et al. A systematic meta-analysis of genetic association studies for diabetic retinopathy[J]. Diabetes, 2009, 58(9): 2137-2147. DOI: 10.2337/db09-0059.
2. Waddington CH. The epigenotype 1942[J]. Int J Epidemiol, 2012, 41(1): 10-13. DOI: 10.1093/ije/dyr184.
3. Portela A, Esteller M. Epigenetic modifications and human disease[J]. Nat Biotechnol, 2010, 28(10): 1057-1068. DOI: 10.1038/nbt.1685.
4. Perrone L, Devi TS, Hosoya K, et al. Thioredoxin interacting protein (TXNIP) induces inflammation through chromatin modification in retinal capillary endothelial cells under diabetic conditions[J]. J Cell Physiol, 2009, 221(1): 262-272. DOI: 10.1002/jcp.21852.
5. Kadiyala CS, Zheng L, Du Y, et al. Acetylation of retinal histones in diabetes increases inflammatory proteins: effects of minocycline and manipulation of histone acetyltransferase (HAT) and histone deacetylase (HDAC)[J]. J Biol Chem, 2012, 287(31): 25869-25880. DOI: 10.1074/jbc.M112.375204.
6. Herencia-Bueno KE, Aldrovani M, Crivelaro RM, et al. Reduction in histone H3 acetylation and chromatin remodeling in corneas of alloxan-induced diabetic rats[J]. Cornea, 2018, 37(5): 624-632. DOI: 10.1097/ICO.0000000000001533.
7. Wu JH, Gao Y, Ren AJ, et al. Altered microRNA expression profiles in retinas with diabetic retinopathy[J]. Ophthalmic Res, 2012, 47(4): 195-201. DOI: 10.1159/000331992.
8. Radović N, Nikolić Jakoba N, Petrović N, et al. MicroRNA-146a and microRNA-155 as novel crevicular fluid biomarkers for periodontitis in non-diabetic and type 2 diabetic patients[J]. J Clin Periodontol, 2018, 45(6): 663-671. DOI: 10.1111/jcpe.12888.
9. Fan B, Luk AOY, Chan JCN, et al. MicroRNA and diabetic complications: a clinical perspective[J]. Antioxid Redox Signal, 2018, 29(11): 1041-1063. DOI: 10.1089/ars.2017.7318.
10. Ungerbäck J, Hosokawa H, Wang X, et al. Pioneering, chromatin remodeling, and epigenetic constraint in early T-cell gene regulation by SPI1 (PU.1)[J]. Genome Res, 2018, 28(10): 1508-1519. DOI: 10.1101/gr.231423.117.
11. Zhong Q, Kowluru RA. Epigenetic changes in mitochondrial superoxide dismutase in the retina and the development of diabetic retinopathy[J]. Diabetes, 2011, 60(4): 1304-1313. DOI: 10.2337/db10-0133.
12. Miao F, Wu X, Zhang L, et al. Genome-wide analysis of histone lysine methylation variations caused by diabetic conditions in human monocytes[J]. J Biol Chem, 2007, 282(18): 13854-13863. DOI: 10.1074/jbc.M609446200.
13. Zhong Q, Kowluru RA. Role of histone acetylation in the development of diabetic retinopathy and the metabolic memory phenomenon[J]. J Cell Biochem, 2010, 110(6): 1306-1313. DOI: 10.1002/jcb.22644.
14. Brasacchio D, Okabe J, Tikellis C, et al. Hyperglycemia induces a dynamic cooperativity of histone methylase and demethylase enzymes associated with gene-activating epigenetic marks that coexist on the lysine tail[J]. Diabetes, 2009, 58(5): 1229-1236. DOI: 10.2337/db08-1666.
15. Deering TG, Ogihara T, Trace AP, et al. Methyltransferase Set7/9 maintains transcription and euchromatin structure at islet-enriched genes[J]. Diabetes, 2009, 58(1): 185-193. DOI: 10.2337/db08-1150.
16. Tewari S, Zhong Q, Santos JM, et al. Mitochondria DNA replication and DNA methylation in the metabolic memory associated with continued progression of diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2012, 53(8): 4881-4888. DOI: 10.1167/iovs.12-9732.
17. Mishra M, Kowluru RA. Epigenetic modification of mitochondrial DNA in the development of diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2015, 56(9): 5133-5142. DOI: 10.1167/iovs.15-16937.
18. Mishra M, Kowluru RA. The role of DNA methylation in the metabolic memory phenomenon associated with the continued progression of diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2016, 57(13): 5748-5757. DOI: 10.1167/iovs.16-19759.
19. Kowluru RA, Shan Y, Mishra M. Dynamic DNA methylation of matrix metalloproteinase-9 in the development of diabetic retinopathy[J]. Lab Invest, 2016, 96(10): 1040-1049. DOI: 10.1038/labinvest.2016.78.
20. Miao F, Gonzalo IG, Lanting L, et al. In vivo chromatin remodeling events leading to inflammatory gene transcription under diabetic conditions[J]. J Biol Chem, 2004, 279(17): 18091-18097. DOI: 10.1074/jbc.M311786200.
21. Xu B, Chiu J, Feng B, et al. PARP activation and the alteration of vasoactive factors and extracellular matrix protein in retina and kidney in diabetes[J]. Diabetes Metab Res Rev, 2008, 24(5): 404-412. DOI: 10.1002/dmrr.842.
22. Gao J, Zheng Z, Gu Q, et al. Deacetylation of MnSOD by PARP-regulated SIRT3 protects retinal capillary endothelial cells from hyperglycemia-induced damage[J]. Biochem Biophys Res Commun, 2016, 472(3): 425-431. DOI: 10.1016/j.bbrc.2015.12.037.
23. Zhong Q, Kowluru RA. Epigenetic modification of Sod2 in the development of diabetic retinopathy and in the metabolic memory: role of histone methylation[J]. Invest Ophthalmol Vis Sci, 2013, 54(1): 244-250. DOI: 10.1167/iovs.12-10854.
24. Ye P, Liu J, He F, et al. Hypoxia-induced deregulation of miR-126 and its regulative effect on VEGF and MMP-9 expression[J]. Int J Med Sci, 2013, 11(1): 17-23. DOI: 10.7150/ijms.7329.
25. Li EH, Huang QZ, Li GC, et al. Effects of miRNA-200b on the development of diabetic retinopathy by targeting VEGFA gene[J/OL]. Biosci Rep, 2017, 37(2): BSR20160572[2017-04-30]. http://www.bioscirep.org/cgi/pmidlookup?view=long&pmid=28122882. DOI: 10.1042/BSR20160572.
26. Kovacs B, Lumayag S, Cowan C, et al. MicroRNAs in early diabetic retinopathy in streptozotocin-induced diabetic rats[J]. Invest Ophthalmol Vis Sci, 2011, 52(7): 4402-4409. DOI: 10.1167/iovs.10-6879.
27. Ling S, Birnbaum Y, Nanhwan MK, et al. MicroRNA-dependent cross-talk between VEGF and HIF1α in the diabetic retina[J]. Cell Signal, 2013, 25(12): 2840-2847. DOI: 10.1016/j.cellsig.2013.08.039.
28. Haque R, Hur EH, Farrell AN, et al. MicroRNA-152 represses VEGF and TGFβ1 expressions through post-transcriptional inhibition of (Pro)renin receptor in human retinal endothelial cells[J]. Mol Vis, 2015, 21: 224-235.
29. Pirola L. The DCCT/EDIC study: epigenetic clues after three decades[J]. Diabetes, 2014, 63(5): 1460-1462. DOI: 10.2337/db14-0238.
30. Diabetes Control and Complications Trial (DCCT)/Epidemiology of Diabetes Interventions and Complications (EDIC) Research Group, Lachin JM, White NH, et al. Effect of intensive diabetes therapy on the progression of diabetic retinopathy in patients with type 1 diabetes: 18 years of follow-up in the DCCT/EDIC[J]. Diabetes, 2015, 64(2): 631-642. DOI: 10.2337/db14-0930.
31. Chen Z, Miao F, Paterson AD, et al. Epigenomic profiling reveals an association between persistence of DNA methylation and metabolic memory in the DCCT/EDIC type 1 diabetes cohort[J]. Proc Natl Acad Sci USA, 2016, 113(21): 3002-3011. DOI: 10.1073/pnas.1603712113.
32. Miao F, Chen Z, Genuth S, et al. Evaluating the role of epigenetic histone modifications in the metabolic memory of type 1 diabetes[J]. Diabetes, 2014, 63(5): 1748-1762. DOI: 10.2337/db13-1251.
33. Kowluru RA, Chan PS. Metabolic memory in diabetes – from in vitro oddity to in vivo problem: role of apoptosis[J]. Brain Res Bull, 2010, 81(2-3): 297-302. DOI: 10.1016/j.brainresbull.2009.05.006.
34. Kowluru RA, Kanwar M, Kennedy A. Metabolic memory phenomenon and accumulation of peroxynitrite in retinal capillaries[J]. Exp Diabetes Res, 2007, 2007: 21976. DOI: 10.1155/2007/21976.
35. Kanwar M, Kowluru RA. Role of glyceraldehyde 3-phosphate dehydrogenase in the development and progression of diabetic retinopathy[J]. Diabetes, 2009, 58(1): 227-234. DOI: 10.2337/db08-1025.
36. Berthiaume M, Boufaied N, Moisan A, et al. High levels of oxidative stress globally inhibit gene transcription and histone acetylation[J]. DNA Cell Biol, 2006, 25(2): 124-134. DOI: 10.1089/dna.2006.25.124.
37. Liu W, Cui Y, Ren W, et al. Epigenetic biomarker screening by FLIM-FRET for combination therapy in ER+ breast cancer[J]. Clin Epigenetics, 2019, 11(1): 16. DOI: 10.1186/s13148-019-0620-6.
38. Duan YT, Yang XA, Fang LY, et al. Anti-proliferative and anti-invasive effects of garcinol from Garcinia indica on gallbladder carcinoma cells[J]. Pharmazie, 2018, 73(7): 413-417. DOI: 10.1691/ph.2018.8366.
39. Di Martile M, Desideri M, De Luca T, et al. Histone acetyltransferase inhibitor CPTH6 preferentially targets lung cancer stem-like cells[J]. Oncotarget, 2016, 7(10): 11332-11348. DOI: 10.18632/oncotarget.7238.
40. Yang Y, Liu K, Liang Y, et al. Histone acetyltransferase inhibitor C646 reverses epithelial to mesenchymal transition of human peritoneal mesothelial cells via blocking TGF-β1/Smad3 signaling pathway in vitro[J]. Int J Clin Exp Pathol, 2015, 8(3): 2746-2754.
41. Gao Y, Zhang C, Chang J, et al. Enzyme-instructed self-assembly of a novel histone deacetylase inhibitor with enhanced selectivity and anticancer efficiency[J/OL]. Biomater Sci, 2019, 2019: E1[2019-01-23]. https://doi.org/10.1039/c8bm01422a. DOI: 10.1039/c8bm01422a. [published online ahead of print].
42. Takai N, Ueda T, Nishida M, et al. A novel histone deacetylase inhibitor, Scriptaid, induces growth inhibition, cell cycle arrest and apoptosis in human endometrial cancer and ovarian cancer cells[J]. Int J Mol Med, 2006, 17(2): 323-329.
43. Hakami NY, Dusting GJ, Peshavariya HM. Trichostatin A, a histone deacetylase inhibitor suppresses NADPH oxidase 4-derived redox signalling and angiogenesis[J]. J Cell Mol Med, 2016, 20(10): 1932-1944. DOI: 10.1111/jcmm.12885.
44. Crosson CE, Mani SK, Husain S, et al. Inhibition of histone deacetylase protects the retina from ischemic injury[J]. Invest Ophthalmol Vis Sci, 2010, 51(7): 3639-3645. DOI: 10.1111/jcmm.12885.

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