Adverse epigenetic signatures by histone methyltransferase set7 contribute to vascular dysfunction in patients with type 2 diabetes mellitus

Circulation: Cardiovascular Genetics

Volumn 8, Issue 1, 2015, Pages 150-158

  Paneni, Francesco ^a   Costantino, Sarah ^a   Battista, Rodolfo ^b   Castello, Lorenzo ^c   Capretti, Giuliana ^c   Chiandotto, Sergio ^c   Scavone, Giuseppe ^d   Villano, Angelo ^d   Pitocco, Dario ^d   Lanza, Gaetano ^d   Volpe, Massimo ^c,e   Lüscher, Thomas F ^f   Cosentino, Francesco ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b Civil Hospital   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d CATHOLIC UNIVERSITY   (Italy)

^e IRCCS NEUROMED   (Italy)

^f UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

Diabetes mellitus; Epigenomics; Inflammation; Oxidative stress

Indexed keywords

8 ISOPROSTAGLANDIN F2 ALPHA; CYCLOOXYGENASE 2; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HISTONE H3; HISTONE METHYLTRANSFERASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; MONOCYTE CHEMOTACTIC PROTEIN 1; HISTONE LYSINE METHYLTRANSFERASE; RELA PROTEIN, HUMAN; SETD7 PROTEIN, HUMAN; TRANSCRIPTION FACTOR RELA;

ADULT; ARTERY DILATATION; ARTICLE; BRACHIAL ARTERY; CLINICAL ARTICLE; CONTROLLED STUDY; EPIGENETICS; FEMALE; HUMAN; HUMAN CELL; INFLAMMATION; MALE; MIDDLE AGED; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATIVE STRESS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; VASCULAR DISEASE; AGED; CELL CULTURE; CLINICAL TRIAL; DIABETIC ANGIOPATHY; ENDOTHELIUM CELL; ENZYMOLOGY; GENETIC EPIGENESIS; GENETICS; METABOLISM; PROMOTER REGION;

ADULT; AGED; CELLS, CULTURED; DIABETES MELLITUS, TYPE 2; DIABETIC ANGIOPATHIES; ENDOTHELIAL CELLS; EPIGENESIS, GENETIC; FEMALE; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; MALE; MIDDLE AGED; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTOR RELA;

EID: 84924627239     PISSN: 1942325X     EISSN: 19423268     Source Type: Journal    
DOI: 10.1161/CIRCGENETICS.114.000671     Document Type: Article

References (34)

1. Beckman JA, Paneni F, Cosentino F, Creager MA. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part II. Eur Heart J. 2013;34:2444-2452. doi: 10.1093/eurheartj/eht142.
2. Hossain P, Kawar B, El Nahas M. Obesity and diabetes in the developing world-a growing challenge. N Engl J Med. 2007;356:213-215. doi: 10.1056/NEJMp068177.
3. Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res. 2010;107:1058-1070. doi: 10.1161/CIRCRESAHA.110.223545.
4. Fioretto P, Dodson PM, Ziegler D, Rosenson RS. Residual microvascular risk in diabetes: unmet needs and future directions. Nat Rev Endocrinol. 2010;6:19-25. doi: 10.1038/nrendo.2009.213.
5. Paneni F, Beckman JA, Creager MA, Cosentino F. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I. Eur Heart J. 2013;34:2436-2443. doi: 10.1093/eurheartj/eht149.
6. Handy DE, Castro R, Loscalzo J. Epigenetic modifications: basic mechanisms and role in cardiovascular disease. Circulation. 2011;123:2145-2156. doi: 10.1161/CIRCULATIONAHA.110.956839.
7. Cooper ME, El-Osta A. Epigenetics: mechanisms and implications for diabetic complications. Circ Res. 2010;107:1403-1413. doi: 10.1161/CIRCRESAHA.110.223552.
8. Okabe J, Orlowski C, Balcerczyk A, Tikellis C, Thomas MC, Cooper ME, et al. Distinguishing hyperglycemic changes by Set7 in vascular endothelial cells. Circ Res. 2012;110:1067-1076. doi: 10.1161/CIRCRESAHA.112.266171.
9. El-Osta A, Brasacchio D, Yao D, Pocai A, Jones PL, Roeder RG, et al. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med. 2008;205:2409-2417. doi: 10.1084/jem.20081188.
10. Sun G, Reddy MA, Yuan H, Lanting L, Kato M, Natarajan R. Epigenetic histone methylation modulates fibrotic gene expression. J Am Soc Nephrol. 2010;21:2069-2080. doi: 10.1681/ASN.2010060633.
11. Li Y, Reddy MA, Miao F, Shanmugam N, Yee JK, Hawkins D, 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. doi: 10.1074/jbc.M802800200.
12. Ryden L, Grant PJ, Anker SD, Berne C, Cosentino F, et al Authors/Task Force Members. ESC guidelines on diabetes, pre-diabetes, and cardiovascular diseases developed in collaboration with the EASD: the Task Force on diabetes, pre-diabetes, and cardiovascular diseases of the European Society of Cardiology (ESC) and developed in collaboration with the European Association for the Study of Diabetes (EASD). Eur Heart J. 2013;34:3035-3087.
13. Paneni F, Osto E, Costantino S, Mateescu B, Briand S, Coppolino G, et al. Deletion of the activated protein-1 transcription factor JunD induces oxidative stress and accelerates age-related endothelial dysfunction. Circulation. 2013;127:1229-1240. doi: 10.1161/CIRCULATIONAHA.112.000826.
14. Ghiadoni L, Faita F, Salvetti M, Cordiano C, Biggi A, Puato M, et al. Assessment of flow-mediated dilation reproducibility: a nationwide multicenter study. J Hypertens. 2012;30:1399-1405. doi: 10.1097/HJH.0b013e328353f222.
15. Baker RG, Hayden MS, Ghosh S. NF-κB, inflammation, and metabolic disease. Cell Metab. 2011;13:11-22. doi: 10.1016/j.cmet.2010.12.008.
16. Kim YW, West XZ, Byzova TV. Inflammation and oxidative stress in angiogenesis and vascular disease. J Mol Med (Berl). 2013;91:323-328. doi: 10.1007/s00109-013-1007-3.
17. Hayden MS, Ghosh S. Shared principles in NF-kappaB signaling. Cell. 2008;132:344-362. doi: 10.1016/j.cell.2008.01.020.
18. Kim JK. Endothelial nuclear factor κB in obesity and aging: is endothelial nuclear factor κB a master regulator of inflammation and insulin resistance? Circulation. 2012;125:1081-1083. doi: 10.1161/CIRCULATIONAHA.111.090134.
19. Paneni F, Costantino S, Volpe M, Lüscher TF, Cosentino F. Epigenetic signatures and vascular risk in type 2 diabetes: a clinical perspective. Atherosclerosis. 2013;230:191-197. doi: 10.1016/j.atherosclerosis.2013.07.003.
20. Chen J, Guo Y, Zeng W, Huang L, Pang Q, Nie L, et al. ER stress triggers MCP-1 expression through SET7/9-induced histone methylation in the kidneys of db/db mice. Am J Physiol Renal Physiol. 2014;306:F916-F925. doi: 10.1152/ajprenal.00697.2012.
21. Paneni F. 2013 ESC/EASD guidelines on the management of diabetes and cardiovascular disease: established knowledge and evidence gaps. Diab Vasc Dis Res. 2014;11:5-10. doi: 10.1177/1479164113512859.
22. Tousoulis D, Papageorgiou N, Androulakis E, Siasos G, Latsios G, Tentolouris K, et al. Diabetes mellitus-associated vascular impairment: novel circulating biomarkers and therapeutic approaches. J Am Coll Cardiol. 2013;62:667-676. doi: 10.1016/j.jacc.2013.03.089.
23. Wong WT, Tian XY, Huang Y. Endothelial dysfunction in diabetes and hypertension: cross talk in RAS, BMP4, and ROS-dependent COX-2-derived prostanoids. J Cardiovasc Pharmacol. 2013;61:204-214. doi: 10.1097/FJC.0b013e31827fe46e.
24. Luo S, Lei H, Qin H, Xia Y. Molecular mechanisms of endothelial NO synthase uncoupling. Curr Pharm Des. 2014;20:3548-3553.
25. Libby P, Ridker PM, Hansson GK. Progress and challenges in translating the biology of atherosclerosis. Nature. 2011;473:317-325. doi: 10.1038/nature10146.
26. Mai A. Small-molecule chromatin-modifying agents: therapeutic applications. Epigenomics. 2010;2:307-324. doi: 10.2217/epi.10.7.
27. Xie M, Kong Y, Tan W, May H, Battiprolu PK, Pedrozo Z, et al. Histone deacetylase inhibition blunts ischemia/reperfusion injury by inducing cardiomyocyte autophagy. Circulation. 2014;129:1139-1151. doi: 10.1161/CIRCULATIONAHA.113.002416.
28. Paneni F, Volpe M, Lüscher TF, Cosentino F. SIRT1, p66(Shc), and Set7/9 in vascular hyperglycemic memory: bringing all the strands together. Diabetes. 2013;62:1800-1807. doi: 10.2337/db12-1648.
29. Zheng Z, Chen H, Li J, Li T, Zheng B, Zheng Y, et al. Sirtuin 1-mediated cellular metabolic memory of high glucose via the LKB1/AMPK/ROS pathway and therapeutic effects of metformin. Diabetes. 2012;61:217-228. doi: 10.2337/db11-0416.
30. Timmers S, Konings E, Bilet L, Houtkooper RH, van de Weijer T, Goossens GH, et al. Calorie restriction-like effects of 30 days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans. Cell Metab. 2011;14:612-622. doi: 10.1016/j.cmet.2011.10.002.
31. Paneni F, Mocharla P, Akhmedov A, Costantino S, Osto E, Volpe M, et al. Gene silencing of the mitochondrial adaptor p66(Shc) suppresses vascular hyperglycemic memory in diabetes. Circ Res. 2012;111:278-289. doi: 10.1161/CIRCRESAHA.112.266593.
32. Ceriello A, Ihnat MA, Thorpe JE. Clinical review 2: The "metabolic memory": is more than just tight glucose control necessary to prevent diabetic complications? J Clin Endocrinol Metab. 2009;94:410-415. doi: 10.1210/jc.2008-1824.
33. Hartman ML, Shirihai OS, Holbrook M, Xu G, Kocherla M, Shah A, et al. Relation of mitochondrial oxygen consumption in peripheral blood mononuclear cells to vascular function in type 2 diabetes mellitus. Vasc Med. 2014;19:67-74. doi: 10.1177/1358863X14521315.
34. Kizhakekuttu TJ, Wang J, Dharmashankar K, Ying R, Gutterman DD, Vita JA, et al. Adverse alterations in mitochondrial function contribute to type 2 diabetes mellitus-related endothelial dysfunction in humans. Arterioscler Thromb Vasc Biol. 2012;32:2531-2539. doi: 10.1161/ATVBAHA.112.256024.