Сахарный диабет и атеросклероз: эпигенетические механизмы патогенеза. Обзор литературы

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L. K. Sokolova
V. M. Pushkarev
O. I. Kovzun
V. V. Pushkarev
M. D. Tronko

Анотація

В обзоре литературы обобщен и проанализирован материал, посвященный эпигенетическим изменениям, сопровождающим сердечно-сосудистые осложнения при сахарном диабете. Представлены данные об участии эпигенетических модификаций в патологических изменениях клеток эндотелия, гладкомышечной мускулатуры и макрофагов, ведущих к атеросклерозу. Описана роль различных микроРНК в дифференцировке, активации, воспалении, пролиферации и миграции клеток сосудов. Показано, что модификации гистонов, метилирование ДНК и изменение спектра микроРНК участвуют в инициации и развитии сердечно-сосудистых заболеваний при сахарном диабете, а их изучение и применение полученных знаний имеет большой диагностический, прогностический, а в перспективе и терапевтический потенциал.

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Ключові слова:

атеросклероз, сахарный диабет, эпигенетические модификации, микроРНК

Посилання

Asgeirsdottir S.A., van Solingen C., Kurniati N.F. et al. MicroRNA-126 contributes to renal microvascular heterogeneity of VCAM-1 protein expression in acute inflammation // Am. J. Physiol. Renal Physiol.– 2012.– Vol. 302.– P. F1630–F1639.

Baker R.G., Hayden M.S., Ghosh S. NF-kappaB, inflammation, and metabolic disease // Cell. Metab.– 2011.– Vol. 13 (1).– P. 11–22.

Bannister A.J., Kouzarides T. Regulation of chromatin by histone modifications // Cell Res.– 2011.– Vol. 21 (3).– P. 381–395.

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 // Diabetes.– 2009.– Vol. 58 (5).– P. 1229–1236.

Cash H.L., Mcgarvey S.T., Houseman E.A. et al. Cardiovascular disease risk factors and DNA methylation at the LINE-1 repeat region in peripheral blood from Samoan Islanders // Epigenetics.– 2011.– Vol. 6 (10).– P. 1257–1264.

Caporali A., Meloni M., Vollenkle C. et al. Deregulation of microRNA-503 contributes to diabetes mellitus-induced impairment of endothelial function and reparative angiogenesis after limb ischemia // Circulation.– 2011.– Vol. 123 (3).– P. 282–291.

Chamorro-Jorganes A., Araldi E., Penalva L.O. et al. MicroRNA-16 and microRNA-424 regulate cell-autonomous angiogenic functions in endothelial cells via targeting vascular endothelial growth factor receptor-2 and fibroblast growth factor receptor-1 // Arterioscler. Thromb. Vasc. Biol.– 2011.– Vol. 31.– P. 2595–2606.

Choe N., Kwon J.S., Kim J.R. et al. The microRNA miR-132 targets Lrrfip1 to block vascular smooth muscle cell proliferation and neointimal hyperplasia // Atherosclerosis.– 2013.– Vol. 229.– P. 348–355.

Choe N., Kwon J.S., Kim Y.S. et al. The microRNA miR-34c inhibits vascular smooth muscle cell proliferation and neointimal hyperplasia by targeting stem cell factor // Cell. Signal.– 2015.– Vol. 27.– P. 1056–1065.

Donners M.M., Wolfs I.M., Stoger L.J. et al. Hematopoietic miR155 deficiency enhances atherosclerosis and decreases plaque stability in hyperlipidemic mice // PLoS One.– 2012.– Vol. 7.– P. e35877.

Du F., Yu F., Wang Y. et al. MicroRNA-155 deficiency results in decreased macrophage inflammation and attenuated atherogenesis in apolipoprotein E-deficient mice // Arterioscler. Thromb. Vasc. Biol.– 2014.– Vol. 34.– P. 759–767.

Dunn J., Simmons R., Thabet S., Jo H. The role of epigenetics in the endothelial cell shear stress response and atherosclerosis // Int. J. Biochem. Cell Biol.– 2015.– Vol. 67.– P. 167–176.

Fang F., Yang Y., Yuan Z. et al. Myocardin-related transcription factor A mediates oxLDL-induced endothelial injury // Circ. Res.– 2011.– Vol. 108 (7).– P. 797–807.

Fang Y., Davies P.F. Site-specific microRNA-92a regulation of Kruppel-like factors 4 and 2 in atherosusceptible endothelium // Arterioscler. Thromb. Vasc. Biol.– 2012.– Vol. 32.– P. 979–987.

Fichtlscherer S., De Rosa S., Fox H. et al. Circulating microRNAs in patients with coronary artery disease // Circ. Res.– 2010.– Vol. 107 (5).– P. 677–684.

Findeisen H.M., Gizard F., Zhao Y. et al. Epigenetic regulation of vascular smooth muscle cell proliferation and neointima formation by histone deacetylase inhibition // Arterioscler. Thromb. Vasc. Biol.– 2011.– Vol. 31 (4).– P. 851–860.

Forrest A.R., Kanamori-Katayama M., Tomaru Y. et al. Induction of microRNAs, mir-155, mir-222, mir-424 and mir-503, promotes monocytic differentiation through combinatorial regulation // Leukemia.– 2010.– Vol. 24.– P. 460–466.

Gao Y., Peng J., Ren Z. et al. Functional regulatory roles of microRNAs in atherosclerosis // Clin. Chim. Acta.– 2016.– Vol. 460.– P. 164–171.

Goettsch C., Rauner M., Pacyna N. et al. miR-125b regulates calcification of vascular smooth muscle cells // Am. J. Pathol.– 2011.– Vol. 179.– P. 1594–1600.

Guay S.P., Brisson D., Lamarche B. et al. DNA methylation variations at CETP and LPL gene promoter loci: new molecular biomarkers associated with blood lipid profile variability // Atherosclerosis.– 2013.– Vol. 228 (2).– P. 413–420.

Hu Y.W., Zhao J.Y., Li S.F. et al. RP5-833A20.1/miR-382-5p/NFIA-dependent signal transduction pathway contributes to the regulation of cholesterol homeostasis and inflammatory reaction // Arterioscler. Thromb. Vasc. Biol.– 2015.– Vol. 35.– P. 87–101.

Huang R.S., Hu G.Q., Lin B. et al. MicroRNA-155 silencing enhances inflammatory response and lipid uptake in oxidized low-density lipoprotein-stimulated human THP-1 macrophages // J. Invest. Med.– 2010.– Vol. 58.– P. 961–967.

Iaconetti C., De Rosa S., Polimeni A. et al. Down-regulation of miR-23b induces phenotypic switching of vascular smooth muscle cells in vitro and in vivo // Cardiovasc. Res.– 2015.– Vol. 107.– P. 522–533.

Illingworth R., Kerr A., Desousa D. et al. A novel CpG island set identifies tissue-specific methylation at developmental gene loci // PLoS Biol.– 2008.– Vol. 6.– P. e22.

Jia L., Zhu L., Wang J.Z. et al. Methylation of FOXP3 in regulatory T cells is related to the severity of coronary artery disease // Atherosclerosis.– 2013.– Vol. 228 (2).– P. 346–352.

Jones P.A. Functions of DNA methylation: islands, start sites, gene bodies and beyond // Nat. Rev. Genet.– 2012.– Vol. 13 (7).– P. 484–492.

Kee H.J., Kim G.R., Cho S.N. et al. MiR-18a-5p microRNA increases vascular smooth muscle cell differentiation by down­­regulating Syndecan4 // Korean Circ. J.– 2014.– Vol. 44.– P. 255–263.

Kim M.H., Ham O., Lee S.Y. et al. MicroRNA-365 inhibits the proliferation of vascular smooth muscle cells by targeting cyclin D1 // J. Cell. Biochem.– 2014.– Vol. 115.– P. 1752–1761.

Kohli R.M., Zhang Y. TET enzymes, TDG and the dynamics of DNA demethylation // Nature.– 2013.– Vol. 502 (7472).– P. 472–479.

Kong X., Fang M., Li P. et al. HDAC2 deacetylates class II transactivator and suppresses its activity in macrophages and smooth muscle cells // J. Mol. Cell. Cardiol.– 2009.– Vol. 46 (3).– P. 292–299.

Kumar A., Kumar S., Vikram A. et al. Histone and DNA methylation-mediated epigenetic downregulation of endothelial Kruppel-like factor 2 by low-density lipoprotein cholesterol // Arterioscler. Thromb. Vasc. Biol.– 2013.– Vol. 33 (8).– P. 1936–1942.

Leeper N.J., Raiesdana A., Kojima Y. et al. MicroRNA-26a is a novel regulator of vascular smooth muscle cell function // J. Cell. Physiol.– 2011.– Vol. 226.– P. 1035–1043.

Li P., Liu Y., Yi B. et al. MicroRNA-638 is highly expressed in human vascular smooth muscle cells and inhibits PDGF-BB-induced cell proliferation and migration through targeting orphan nuclear receptor NOR1 // Cardiovasc. Res.– 2013.– Vol. 99.– P. 185–193.

Li P., Zhu N., Yi B. et al. MicroRNA-663 regulates human vascular smooth muscle cell phenotypic switch and vascular neointimal formation // Circ. Res.– 2013.– Vol. 113.– P. 1117–1127.

Li Q., Chen L., Chen D. et al. Influence of microRNA-related polymorphisms on clinical outcomes in coronary artery disease // Am. J. Transl. Res.– 2015.– Vol. 7 (2).– P. 393–400.

Liao X.B., Zhang Z.Y., Yuan K. et al. MiR-133a modulates osteogenic differentiation of vascular smooth muscle cells // Endo­­crinology.– 2013.– Vol. 154.– P. 3344–3352.

Lin H.S., Gong J.N., Su R. et al. miR-199a-5p inhibits monocyte/macrophage differentiation by targeting the activin a type 1B receptor gene and finally reducing C/EBPalpha expression // J. Leukoc. Biol.– 2014.– Vol. 96.– P. 1023–1035.

Liu Y., Pan Q., Zhao Y. et al. MicroRNA-155 regulates ROS production, no generation, apoptosis and multiple functions of human brain microvessel endothelial cells under physiological and pathological conditions // J. Cell. Biochem.– 2015.– Vol. 116.– P. 2870–2881.

Lovren F., Pan Y., Quan A. et al. MicroRNA-145 targeted therapy reduces atherosclerosis // Circulation.– 2012.– Vol. 126.– P. S81–S90.

Lynch M., Barallobre-Barreiro J., Jahangiri M., Mayr M. Vascular proteomics in metabolic and cardiovascular diseases // J. Intern. Med.– 2016.– Vol. 280 (4).– P. 325–338.

Madrigal-Matute J., Rotllan N., Aranda J.F., Fernández-Hernando C. MicroRNAs and atherosclerosis // Curr. Atheroscler. Rep.– 2013.– Vol. 15 (5).– P. 322.

Mcdonald O.G., Wamhoff B.R., Hoofnagle M.H., Owens G.K. Control of SRF binding to CArG box chromatin regulates smooth muscle gene expression in vivo // J. Clin. Invest.– 2006.– Vol. 116 (1).– P. 36–48.

Menghini R., Casagrande V., Cardellini M. et al. MicroRNA 217 modulates endothelial cell senescence via silent information regulator 1 // Circulation.– 2009.– Vol. 120.– P. 1524–1532.

Menghini R., Casagrande V., Marino A. et al. MiR-216a: a link between endothelial dysfunction and autophagy // Cell Death Dis.– 2014.– Vol. 5.– P. e1029.

Motawae T.M., Ismail M.F., Shabayek M.I., Seleem M.M. MicroRNAs 9 and 370 association with biochemical markers in T2D and CAD complication of T2D // PLoS ONE.– 2015.– Vol. 10 (5).– P. e0126957.

Nazari-Jahantigh M., Egea V., Schober A., Weber C. MicroRNA-specific regulatory mechanisms in atherosclerosis // J. Mol. Cell. Cardiol.– 2015.– Vol. 89 (Pt A).– P. 35–41.

Niu P.P., Cao Y., Gong T. et al. Hypermethylation of DDAH2 promoter contributes to the dysfunction of endothelial progenitor cells in coronary artery disease patients // J. Transl. Med.– 2014.– Vol. 12.– P. 170.

Orom U.A., Shiekhattar R. Long noncoding RNAs usher in a new era in the biology of enhancers // Cell.– 2013.– Vol. 154 (6).– P. 1190–1193.

Ouimet M., Ediriweera H.N., Gundra U.M. et al. MicroRNA-33-dependent regulation of macrophage metabolism directs immune cell polarization in atherosclerosis // J. Clin. Invest.– 2015.– Vol. 125 (12).– P. 4334–4448.

Pasquier J., Hoarau-Véchot J., Fakhro K. et al. Epigenetics and cardiovascular disease in diabetes // Curr. Diab. Rep.– 2015.– Vol. 15 (12).– P. 108.

Pirola L., Balcerczyk A., Tothill R.W. et al. Genome-wide analysis distinguishes hyperglycemia regulated epigenetic signatures of primary vascular cells // Genome Res.– 2011.– Vol. 21 (10).– P. 1601–1615.

Qi L., Zhi J., Zhang T. et al. Inhibition of microRNA-25 by tumor necrosis factor alpha is critical in the modulation of vascular smooth muscle cell proliferation // Mol. Med. Rep.– 2015.– Vol. 11.– P. 4353–4358.

Ruparelia N., Chai J.T., Fisher E.A., Choudhury R.P. Inflammatory processes in cardiovascular disease: a route to targeted therapies // Nat. Rev. Cardiol.– 2017.– Vol. 14 (3).– P. 133–144.

Schober A., Nazari-Jahantigh M., Wei Y. et al. MicroRNA-126-5p promotes endothelial proliferation and limits atherosclerosis by suppressing Dlk1 // Nat. Med.– 2014.– Vol. 20.– P. 368–376.

Siemelink M., Van Der Laan S., Timmers L. et al. Taking risk prediction to the next level. Advances in biomarker research for atherosclerosis // Curr. Pharm. Des.– 2013.– Vol. 19 (33).– P. 5929–5941.

Siracuse J.J., Chaikof E.L. The Pathogenesis of diabetic atherosclerosis // Diabetes and peripheral vascular disease / Eds. G.V. Shrikhande, J.F. McKinsey.– N.-Y., 2012.– 243 p.

Stather P.W., Sylvius N., Wild J.B. et al. Differential microRNA expression profiles in peripheral arterial disease // Circ. Cardiovasc. Genet.– 2013.– Vol. 6 (5).– P. 490–497.

Sun Y., Chen D., Cao L. et al. MiR-490-3p modulates the proliferation of vascular smooth muscle cells induced by oxLDL through targeting PAPP-A // Cardiovasc. Res.– 2013.– Vol. 100.– P. 272–279.

von der Thusen J.H., Borensztajn K.S., Moimas S. et al. IGF-1 has plaque-stabilizing effects in atherosclerosis by altering vascular smooth muscle cell phenotype // Am. J. Pathol.– 2011.– Vol. 178.– P. 924–934.

Togliatto G., Trombetta A., Dentelli P. et al. Unacylated ghrelin induces oxidative stress resistance in a glucose intolerance and peripheral artery disease mouse model by restoring endothelial cell miR-126 expression // Diabetes.– 2015.– Vol. 64.– P. 1370–1382.

Vasa-Nicotera M., Chen H., Tucci P. et al. miR-146a is modulated in human endothelial cell with aging // Atherosclerosis.– 2011.– Vol. 217.– P. 326–330.

Villeneuve L.M., Kato M., Reddy M.A. 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.– Vol. 59 (11).– P. 2904–2915.

Wei Y., Nazari-Jahantigh M., Chan L. et al. The microRNA-342-5p fosters inflammatory macrophage activation through an Akt1- and microRNA-155-dependent pathway during atherosclerosis // Circulation.– 2013.– Vol. 127.– P. 1609–1619.

Wu Y., Huang A., Li t. et al. MiR-152 reduces human umbilical vein endothelial cell proliferation and migration by targeting ADAM17 // FEBS Lett.– 2014.– Vol. 588.– P. 2063–2069.

Xiao L., Liu Y., Wang N. New paradigms in inflammatory signaling in vascular endothelial cells // Am. J. Physiol. Heart Circ. Physiol.– 2014.– Vol. 306 (3).– P. H317–H325.

Xie B., Zhang C., Kang K., Jiang S. MiR-599 inhibits vascular smooth muscle cells proliferation and migration by targeting TGFB2 // PLoS One.– 2015.– Vol. 10.– P. e0141512.

Xu Q., Meng S., Liu B. et al. MicroRNA-130a regulates autophagy of endothelial progenitor cells through Runx3 // Clin. Exp. Pharmacol. Physiol.– 2014.– Vol. 41.– P. 351–357.

Xu Z., Han Y., Liu J. et al. MiR-135b-5p and MiR-499a-3p promote cell proliferation and migration in atherosclerosis by directly targeting MEF2C // Sci. Rep.– 2015.– Vol. 5.– P. 12276.

Yamada Y., Nishida T., Horibe H. et al. Identification of hypo- and hypermethylated genes related to atherosclerosis by a genome-wide analysis of DNA methylation // Int. J. Mol. Med.– 2014.– Vol. 33 (5).– P. 1355–1363.

Yamakuchi M. Endothelial senescence and microRNA // Biomol. Concepts.– 2012.– Vol. 3.– P. 213–223.

Yamamoto S., Narita I., Kotani K. The macrophage and its related cholesterol efflux as a HDL function index in atherosclerosis // Clin. Chim. Acta.– 2016.– Vol. 457.– P. 117–122.

Zhang B.K., Lai X., Jia S.J. Epigenetics in atherosclerosis: a clinical perspective // Discov. Med.– 2015.– Vol. 19 (103).– P. 73–80.

Zhang T., Tian F., Wang J. et al. Endothelial cell autophagy in atherosclerosis is regulated by miR-30-mediated translational control of ATG6 // Cell. Physiol. Biochem.– 2015.– Vol. 37.– P. 1369–1378.

Zhang Y., Liu D., Chen X. et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration // Mol. Cell.– 2010.– Vol. 39.– P. 133–144.

Zhang Y., Zeng C. Role of DNA methylation in cardiovascular diseases // Clin. Exp. Hypertens.– 2016.– Vol. 38 (3).– P. 261–267.

Zhou B., Margariti A., Zeng L. et al. Splicing of histone deacetylase 7 modulates smooth muscle cell proliferation and neointima formation through nuclear beta-catenin translocation // Arterioscler. Thromb. Vasc. Biol.– 2011.– Vol. 31 (11).– P. 2676–2684.

Zhou S., Chen H.Z., Wan Y.Z. et al. Repression of P66Shc expression by SIRT1 contributes to the prevention of hyperglycemia-induced endothelial dysfunction // Circ. Res.– 2001.– Vol. 109 (6).– P. 639–648.

Zhu J., Chen T., Yang L. et al. Regulation of microRNA-155 in atherosclerotic inflammatory responses by targeting MAP3K10 // PLoS One.– 2012.– Vol. 7.– P. e46551.

Zhu N., Zhang D., Chen S. et al. Endothelial enriched microRNAs regulate angiotensin II-induced endothelial inflammation and migration // Atherosclerosis.– 2011.– Vol. 215.– P. 286–293.

Zhuang Y., Peng H., Mastej V., Chen W. MicroRNA regulation of endothelial junction proteins and clinical consequence // Mediators Inflamm.– 2016.– Vol. 2016.– P. 5078627.