Research progress of epigenetic regulation of vascular diseases_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

LI Dongze ^1,2 , LI Fanghui ³ , ZENG Rui ³ , CAO Yu ^1,2 ,  WAN Zhi ^1,2

1. Department of Emergency Medicine, West China Hospital, Sichuan University, Chengdu, 610041, P.R.China;
2. Disaster Medical Center, Sichuan University, Chengdu, 610041, P.R.China;
3. Department of Cardiology, West China Hospital, Sichuan University, Chengdu, 610041, P.R.China;

Corresponding author：

WAN Zhi, Email: 303680215@qq.com

Keywords：

Vascular diseases; TET methylcytosine dioxygenase 2; epigenetics

DOI：

10.7507/1007-4848.201906072

Video：

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Epigenetics refers to heritable changes in gene expression independent of DNA nucleotide sequence itself, and the main mechanisms include DNA methylation, histone modifications, noncoding RNAs, and so on. Vascular disease is a chronic disease regulated by the interaction between environmental and genetic factors. In recent years, more and more studies have confirmed that epigenetic regulation plays an important role in the occurrence and development of vascular diseases. This article reviews recent advances in epigenetics in vascular disease.

Citation： LI Dongze, LI Fanghui, ZENG Rui, CAO Yu, WAN Zhi. Research progress of epigenetic regulation of vascular diseases. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2020, 27(4): 471-475. doi: 10.7507/1007-4848.201906072 Copy

1.	Lorenzen JM, Martino F, Thum T. Epigenetic modifications in cardiovascular disease. Basic Res Cardiol, 2012, 107(2): 245.
2.	Mazzio EA, Soliman KF. Basic concepts of epigenetics: impact of environmental signals on gene expression. Epigenetics, 2012, 7(2): 119-130.
3.	Jones MJ, Goodman SJ, Kobor MS. DNA methylation and healthy human aging. Aging Cell, 2015, 14(6): 924-932.
4.	Sharma S, Kelly TK, Jones PA. Epigenetics in cancer. Carcinogenesis, 2010, 31(1): 27-36.
5.	Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol, 2010, 28(10): 1057-1068.
6.	Tammen SA, Friso S, Choi SW. Epigenetics: the link between nature and nurture. Mol Aspects Med, 2013, 34(4): 753-764.
7.	Dor Y, Cedar H. Principles of DNA methylation and their implications for biology and medicine. Lancet, 2018, 392(10149): 777-786.
8.	Andersen GB, Tost J. A summary of the biological processes, disease-associated changes, and clinical applications of DNA methylation. Methods Mol Biol, 2018, 1708: 3-30.
9.	张又嘉, 陈宇虹, 雷苑. 表观遗传调控与青光眼发病机制研究进展. 眼科新进展, 2019, 39(5): 477-481.
10.	Traube FR, Carell T. The chemistries and consequences of DNA and RNA methylation and demethylation. RNA Biol, 2017, 14(9): 1099-1107.
11.	陈悦, 李杰, 陈伶利, 等. 冠心病血瘀证与 DNA 甲基化/羟甲基化关系及研究进展. 湖南中医药大学学报, 2018, 38(9): 1077-1081.
12.	Zhuang J, Luan P, Li H, et al. The Yin-Yang dynamics of DNA methylation is the key regulator for smooth muscle cell phenotype switch and vascular remodeling. Arterioscler Thromb Vasc Biol, 2017, 37(1): 84-97.
13.	Kolendowski B, Hassan H, Krstic M, et al. Genome-wide analysis reveals a role for TDG in estrogen receptor-mediated enhancer RNA transcription and 3-dimensional reorganization. Epigenetics Chromatin, 2018, 11(1): 5.
14.	Cheng YW, Chou CJ, Yang PM. Ten-eleven translocation 1 (TET1) gene is a potential target of miR-21-5p in human colorectal cancer. Surg Oncol, 2018, 27(1): 76-81.
15.	Chen QW, Zhu XY, Li YY, et al. Epigenetic regulation and cancer (review). Oncol Rep, 2014, 31(2): 523-532.
16.	Perri F, Longo F, Giuliano M, et al. Epigenetic control of gene expression: Potential implications for cancer treatment. Crit Rev Oncol Hematol, 2017, 111: 166-172.
17.	Kouzarides T. Chromatin modifications and their function. Cell, 2007, 128(4): 693-705.
18.	李芳卉, 李东泽, 张蜀. 微小 RNA 和长链非编码 RNA 作为心脏疾病生物标志物的研究进展. 中国循环杂志, 2017, 32(11): 1131-1133.
19.	Gangwar RS, Rajagopalan S, Natarajan R, et al. Noncoding RNAs in cardiovascular disease: pathological relevance and emerging role as biomarkers and therapeutics. Am J Hypertens, 2018, 31(2): 150-165.
20.	Zdravkovic S, Wienke A, Pedersen NL, et al. Heritability of death from coronary heart disease: a 36-year follow-up of 20 966 Swedish twins. J Intern Med, 2002, 252(3): 247-254.
21.	Khera AV, Emdin CA, Drake I, et al. Genetic risk, adherence to a healthy lifestyle, and coronary disease. N Engl J Med, 2016, 375(24): 2349-2358.
22.	Said MA, Verweij N, van der Harst P. Associations of combined genetic and lifestyle risks with incident cardiovascular disease and diabetes in the UK biobank study. JAMA Cardiol, 2018, 3(8): 693-702.
23.	Sotos-Prieto M, Baylin A, Campos H, et al. Lifestyle cardiovascular risk score, genetic risk score, and myocardial infarction in Hispanic/Latino adults living in Costa Rica. J Am Heart Assoc, 2016, 5(12): pii: e004067.
24.	Prospective Studies Collaboration, Lewington S, Whitlock G, et al. Blood cholesterol and vascular mortality by age, sex, and blood pressure: a meta-analysis of individual data from 61 prospective studies with 55 000 vascular deaths. Lancet, 2007, 370(9602): 1829-1839.
25.	Sniderman AD, Islam S, McQueen M, et al. Age and cardiovascular risk attributable to apolipoprotein B, low-density lipoprotein cholesterol or non-high-density lipoprotein cholesterol. J Am Heart Assoc, 2016, 5(10): pii: e003665.
26.	Cook NR, Buring JE, Ridker PM. The effect of including C-reactive protein in cardiovascular risk prediction models for women. Ann Intern Med, 2006, 145(1): 21-29.
27.	Rulands S, Lee HJ, Clark SJ, et al. Genome-scale oscillations in DNA methylation during exit from pluripotency. Cell Syst, 2018, 7(1): 63-76.
28.	Horvath S. DNA methylation age of human tissues and cell types. Genome Biol, 2013, 14(10): R115.
29.	Heijmans BT, Tobi EW, Stein AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA, 2008, 105(44): 17046-17049.
30.	Javed R, Chen W, Lin F, et al. Infant's DNA methylation age at birth and epigenetic aging accelerators. Biomed Res Int, 2016, 2016: 4515928.
31.	Bekkering S, Blok BA, Joosten LA, et al. In vitro experimental model of trained innate immunity in human primary monocytes. Clin Vaccine Immunol, 2016, 23(12): 926-933.
32.	Miao F, Chen Z, Genuth S, et al. Evaluating the role of epigenetic histone modifcations in the metabolic memory of type 1 diabetes. Diabetes, 2014, 63: 48-62.
33.	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(10): 2409-2417.
34.	Reddy MA, Zhang E, Natarajan R. Epigenetic mechanisms in diabetic complications and metabolic memory. Diabetologia, 2015, 58(3): 443-455.
35.	李芳卉, 李东泽, 曾锐. 微小 RNA 在主动脉瘤中的研究进展. 临床心血管病杂志, 2018, 34: 851-855.
36.	Lino Cardenas CL, Kessinger CW, Cheng Y, et al. An HDAC9-MALAT1-BRG1 complex mediates smooth muscle dysfunction in thoracic aortic aneurysm. Nat Commun, 2018, 9(1): 1009.
37.	Shah AA, Gregory SG, Krupp D, et al. Epigenetic profiling identifies novel genes for ascending aortic aneurysm formation with bicuspid aortic valves. Heart Surg Forum, 2015, 18(4): E134-E139.
38.	Kim CW, Kumar S, Son DJ, et al. Prevention of abdominal aortic aneurysm by anti-microRNA-712 or anti-microRNA-205 in angiotensin Ⅱ-infused mice. Arterioscler Thromb Vasc Biol, 2014, 34(7): 1412-1421.
39.	Jiao T, Yao Y, Zhang B, et al. Role of microRNA-103a targeting ADAM10 in abdominal aortic aneurysm. Biomed Res Int, 2017, 2017: 9645874.
40.	Zampetaki A, Attia R, Mayr U, et al. Role of miR-195 in aortic aneurysmal disease. Circ Res, 2014, 115(10): 857-866.
41.	Fuster JJ, MacLauchlan S, Zuriaga MA, et al. Clonal hematopoiesis associated with TET2 deficiency accelerates atherosclerosis development in mice. Science, 2017, 355(6327): 842-847.
42.	Bennett MR, Sinha S, Owens GK. Vascular smooth muscle cells in atherosclerosis. Circ Res, 2016, 118(4): 692-702.
43.	Peng J, Yang Q, Li AF, et al. Tet methylcytosine dioxygenase 2 inhibits atherosclerosis via upregulation of autophagy in ApoE-/- mice. Oncotarget, 2016, 7(47): 76423-76436.
44.	Li G, Peng J, Liu Y, et al. Oxidized low-density lipoprotein inhibits THP-1-derived macrophage autophagy via TET2 down-regulation. Lipids, 2015, 50(2): 177-183.
45.	International Stroke Genetics Consortium (ISGC), Wellcome Trust Case Control Consortium 2 (WTCCC2), Bellenguez C, et al. Genome-wide association study identifies a variant in HDAC9 associated with large vessel ischemic stroke. Nat Genet, 2012, 44(3): 328-333.
46.	Markus HS, Mäkelä KM, Bevan S, et al. Evidence HDAC9 genetic variant associated with ischemic stroke increases risk via promoting carotid atherosclerosis. Stroke, 2013, 44(5): 1220-1225.
47.	Hai Z, Zuo W. Aberrant DNA methylation in the pathogenesis of atherosclerosis. Clin Chim Acta, 2016, 456: 69-74.
48.	Lövkvist C, Dodd IB, Sneppen K, et al. DNA methylation in human epigenomes depends on local topology of CpG sites. Nucleic Acids Res, 2016, 44(11): 5123-5132.
49.	Hautefort A, Chesné J, Preussner J, et al. Pulmonary endothelial cell DNA methylation signature in pulmonary arterial hypertension. Oncotarget, 2017, 8(32): 52995-53016.
50.	Gamen E, Seeger W, Pullamsetti SS. The emerging role of epigenetics in pulmonary hypertension. Eur Respir J, 2016, 48(3): 903-917.
51.	Leisegang MS, Fork C, Josipovic I, et al. Long noncoding RNA MANTIS facilitates endothelial angiogenic function. Circulation, 2017, 136(1): 65-79.
52.	Neumann P, Jaé N, Knau A, et al. The lncRNA GATA6-AS epigenetically regulates endothelial gene expression via interaction with LOXL2. Nat Commun, 2018, 9(1): 237.
53.	Kim HW, Stansfield BK. Genetic and epigenetic regulation of aortic aneurysms. Biomed Res Int, 2017, 2017: 7268521.
54.	Hwang JY, Aromolaran KA, Zukin RS. Epigenetic mechanisms in stroke and epilepsy. Neuropsychopharmacology, 2013, 38(1): 167-182.
55.	Gal5n M, Varona S, Orriols M, et al. Induction of histone deacetylases (HDACs) in human abdominal aortic aneurysm: therapeutic potential of HDAC inhibitors. Dis Model Mech, 2016, 9(5): 541-552.

1. Lorenzen JM, Martino F, Thum T. Epigenetic modifications in cardiovascular disease. Basic Res Cardiol, 2012, 107(2): 245.
2. Mazzio EA, Soliman KF. Basic concepts of epigenetics: impact of environmental signals on gene expression. Epigenetics, 2012, 7(2): 119-130.
3. Jones MJ, Goodman SJ, Kobor MS. DNA methylation and healthy human aging. Aging Cell, 2015, 14(6): 924-932.
4. Sharma S, Kelly TK, Jones PA. Epigenetics in cancer. Carcinogenesis, 2010, 31(1): 27-36.
5. Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol, 2010, 28(10): 1057-1068.
6. Tammen SA, Friso S, Choi SW. Epigenetics: the link between nature and nurture. Mol Aspects Med, 2013, 34(4): 753-764.
7. Dor Y, Cedar H. Principles of DNA methylation and their implications for biology and medicine. Lancet, 2018, 392(10149): 777-786.
8. Andersen GB, Tost J. A summary of the biological processes, disease-associated changes, and clinical applications of DNA methylation. Methods Mol Biol, 2018, 1708: 3-30.
9. 张又嘉, 陈宇虹, 雷苑. 表观遗传调控与青光眼发病机制研究进展. 眼科新进展, 2019, 39(5): 477-481.
10. Traube FR, Carell T. The chemistries and consequences of DNA and RNA methylation and demethylation. RNA Biol, 2017, 14(9): 1099-1107.
11. 陈悦, 李杰, 陈伶利, 等. 冠心病血瘀证与 DNA 甲基化/羟甲基化关系及研究进展. 湖南中医药大学学报, 2018, 38(9): 1077-1081.
12. Zhuang J, Luan P, Li H, et al. The Yin-Yang dynamics of DNA methylation is the key regulator for smooth muscle cell phenotype switch and vascular remodeling. Arterioscler Thromb Vasc Biol, 2017, 37(1): 84-97.
13. Kolendowski B, Hassan H, Krstic M, et al. Genome-wide analysis reveals a role for TDG in estrogen receptor-mediated enhancer RNA transcription and 3-dimensional reorganization. Epigenetics Chromatin, 2018, 11(1): 5.
14. Cheng YW, Chou CJ, Yang PM. Ten-eleven translocation 1 (TET1) gene is a potential target of miR-21-5p in human colorectal cancer. Surg Oncol, 2018, 27(1): 76-81.
15. Chen QW, Zhu XY, Li YY, et al. Epigenetic regulation and cancer (review). Oncol Rep, 2014, 31(2): 523-532.
16. Perri F, Longo F, Giuliano M, et al. Epigenetic control of gene expression: Potential implications for cancer treatment. Crit Rev Oncol Hematol, 2017, 111: 166-172.
17. Kouzarides T. Chromatin modifications and their function. Cell, 2007, 128(4): 693-705.
18. 李芳卉, 李东泽, 张蜀. 微小 RNA 和长链非编码 RNA 作为心脏疾病生物标志物的研究进展. 中国循环杂志, 2017, 32(11): 1131-1133.
19. Gangwar RS, Rajagopalan S, Natarajan R, et al. Noncoding RNAs in cardiovascular disease: pathological relevance and emerging role as biomarkers and therapeutics. Am J Hypertens, 2018, 31(2): 150-165.
20. Zdravkovic S, Wienke A, Pedersen NL, et al. Heritability of death from coronary heart disease: a 36-year follow-up of 20 966 Swedish twins. J Intern Med, 2002, 252(3): 247-254.
21. Khera AV, Emdin CA, Drake I, et al. Genetic risk, adherence to a healthy lifestyle, and coronary disease. N Engl J Med, 2016, 375(24): 2349-2358.
22. Said MA, Verweij N, van der Harst P. Associations of combined genetic and lifestyle risks with incident cardiovascular disease and diabetes in the UK biobank study. JAMA Cardiol, 2018, 3(8): 693-702.
23. Sotos-Prieto M, Baylin A, Campos H, et al. Lifestyle cardiovascular risk score, genetic risk score, and myocardial infarction in Hispanic/Latino adults living in Costa Rica. J Am Heart Assoc, 2016, 5(12): pii: e004067.
24. Prospective Studies Collaboration, Lewington S, Whitlock G, et al. Blood cholesterol and vascular mortality by age, sex, and blood pressure: a meta-analysis of individual data from 61 prospective studies with 55 000 vascular deaths. Lancet, 2007, 370(9602): 1829-1839.
25. Sniderman AD, Islam S, McQueen M, et al. Age and cardiovascular risk attributable to apolipoprotein B, low-density lipoprotein cholesterol or non-high-density lipoprotein cholesterol. J Am Heart Assoc, 2016, 5(10): pii: e003665.
26. Cook NR, Buring JE, Ridker PM. The effect of including C-reactive protein in cardiovascular risk prediction models for women. Ann Intern Med, 2006, 145(1): 21-29.
27. Rulands S, Lee HJ, Clark SJ, et al. Genome-scale oscillations in DNA methylation during exit from pluripotency. Cell Syst, 2018, 7(1): 63-76.
28. Horvath S. DNA methylation age of human tissues and cell types. Genome Biol, 2013, 14(10): R115.
29. Heijmans BT, Tobi EW, Stein AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA, 2008, 105(44): 17046-17049.
30. Javed R, Chen W, Lin F, et al. Infant's DNA methylation age at birth and epigenetic aging accelerators. Biomed Res Int, 2016, 2016: 4515928.
31. Bekkering S, Blok BA, Joosten LA, et al. In vitro experimental model of trained innate immunity in human primary monocytes. Clin Vaccine Immunol, 2016, 23(12): 926-933.
32. Miao F, Chen Z, Genuth S, et al. Evaluating the role of epigenetic histone modifcations in the metabolic memory of type 1 diabetes. Diabetes, 2014, 63: 48-62.
33. 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(10): 2409-2417.
34. Reddy MA, Zhang E, Natarajan R. Epigenetic mechanisms in diabetic complications and metabolic memory. Diabetologia, 2015, 58(3): 443-455.
35. 李芳卉, 李东泽, 曾锐. 微小 RNA 在主动脉瘤中的研究进展. 临床心血管病杂志, 2018, 34: 851-855.
36. Lino Cardenas CL, Kessinger CW, Cheng Y, et al. An HDAC9-MALAT1-BRG1 complex mediates smooth muscle dysfunction in thoracic aortic aneurysm. Nat Commun, 2018, 9(1): 1009.
37. Shah AA, Gregory SG, Krupp D, et al. Epigenetic profiling identifies novel genes for ascending aortic aneurysm formation with bicuspid aortic valves. Heart Surg Forum, 2015, 18(4): E134-E139.
38. Kim CW, Kumar S, Son DJ, et al. Prevention of abdominal aortic aneurysm by anti-microRNA-712 or anti-microRNA-205 in angiotensin Ⅱ-infused mice. Arterioscler Thromb Vasc Biol, 2014, 34(7): 1412-1421.
39. Jiao T, Yao Y, Zhang B, et al. Role of microRNA-103a targeting ADAM10 in abdominal aortic aneurysm. Biomed Res Int, 2017, 2017: 9645874.
40. Zampetaki A, Attia R, Mayr U, et al. Role of miR-195 in aortic aneurysmal disease. Circ Res, 2014, 115(10): 857-866.
41. Fuster JJ, MacLauchlan S, Zuriaga MA, et al. Clonal hematopoiesis associated with TET2 deficiency accelerates atherosclerosis development in mice. Science, 2017, 355(6327): 842-847.
42. Bennett MR, Sinha S, Owens GK. Vascular smooth muscle cells in atherosclerosis. Circ Res, 2016, 118(4): 692-702.
43. Peng J, Yang Q, Li AF, et al. Tet methylcytosine dioxygenase 2 inhibits atherosclerosis via upregulation of autophagy in ApoE-/- mice. Oncotarget, 2016, 7(47): 76423-76436.
44. Li G, Peng J, Liu Y, et al. Oxidized low-density lipoprotein inhibits THP-1-derived macrophage autophagy via TET2 down-regulation. Lipids, 2015, 50(2): 177-183.
45. International Stroke Genetics Consortium (ISGC), Wellcome Trust Case Control Consortium 2 (WTCCC2), Bellenguez C, et al. Genome-wide association study identifies a variant in HDAC9 associated with large vessel ischemic stroke. Nat Genet, 2012, 44(3): 328-333.
46. Markus HS, Mäkelä KM, Bevan S, et al. Evidence HDAC9 genetic variant associated with ischemic stroke increases risk via promoting carotid atherosclerosis. Stroke, 2013, 44(5): 1220-1225.
47. Hai Z, Zuo W. Aberrant DNA methylation in the pathogenesis of atherosclerosis. Clin Chim Acta, 2016, 456: 69-74.
48. Lövkvist C, Dodd IB, Sneppen K, et al. DNA methylation in human epigenomes depends on local topology of CpG sites. Nucleic Acids Res, 2016, 44(11): 5123-5132.
49. Hautefort A, Chesné J, Preussner J, et al. Pulmonary endothelial cell DNA methylation signature in pulmonary arterial hypertension. Oncotarget, 2017, 8(32): 52995-53016.
50. Gamen E, Seeger W, Pullamsetti SS. The emerging role of epigenetics in pulmonary hypertension. Eur Respir J, 2016, 48(3): 903-917.
51. Leisegang MS, Fork C, Josipovic I, et al. Long noncoding RNA MANTIS facilitates endothelial angiogenic function. Circulation, 2017, 136(1): 65-79.
52. Neumann P, Jaé N, Knau A, et al. The lncRNA GATA6-AS epigenetically regulates endothelial gene expression via interaction with LOXL2. Nat Commun, 2018, 9(1): 237.
53. Kim HW, Stansfield BK. Genetic and epigenetic regulation of aortic aneurysms. Biomed Res Int, 2017, 2017: 7268521.
54. Hwang JY, Aromolaran KA, Zukin RS. Epigenetic mechanisms in stroke and epilepsy. Neuropsychopharmacology, 2013, 38(1): 167-182.
55. Gal5n M, Varona S, Orriols M, et al. Induction of histone deacetylases (HDACs) in human abdominal aortic aneurysm: therapeutic potential of HDAC inhibitors. Dis Model Mech, 2016, 9(5): 541-552.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Research progress of epigenetic regulation of vascular diseases

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