Inhibiting DNA methylation by 5-Aza-2'-deoxycytidine ameliorates atherosclerosis through suppressing macrophage inflammation

Endocrinology

Volumn 155, Issue 12, 2014, Pages 4925-4938

  Cao, Qiang ^a,b   Wang, Xianfeng ^b   Jia, Lin ^c   Mondal, Ashis K ^b   Diallo, Abdoulaye ^b   Hawkins, Gregory A ^b   Das, Swapan K ^b   Parks, John S ^b   Yu, Liqing ^d   Shi, Huidong ^b   Shi, Hang ^a,e   Xue, Bingzhong ^a,b  

^a GEORGIA STATE UNIVERSITY   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS AT DALLAS   (United States)

^d UNIVERSITY OF MARYLAND   (United States)

^e MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZACITIDINE; DECITABINE; LIPID; LIVER X RECEPTOR; ORPHAN NUCLEAR RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ANALOGS AND DERIVATIVES; ANIMAL; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLOOD; CELL ADHESION; CELL CULTURE; CELL MOTION; DNA METHYLATION; ENDOPLASMIC RETICULUM STRESS; GENETICS; KNOCKOUT MOUSE; MACROPHAGE; MALE; MOUSE; PATHOLOGY; PHYSIOLOGY; PROMOTER REGION; RANDOMIZATION; RAT;

ANIMALS; ATHEROSCLEROSIS; AZACITIDINE; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; DNA METHYLATION; ENDOPLASMIC RETICULUM STRESS; LIPIDS; MACROPHAGES; MALE; MICE; MICE, KNOCKOUT; ORPHAN NUCLEAR RECEPTORS; PLAQUE, ATHEROSCLEROTIC; PPAR GAMMA; PROMOTER REGIONS, GENETIC; RANDOM ALLOCATION; RATS;

EID: 84914132768     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1595     Document Type: Article

References (60)

1. Galkina E, Ley K. Immune and inflammatory mechanisms of atherosclerosis (∗). Annu Rev Immunol. 2009;27:165-197.
2. Libby P, Ridker PM, Hansson GK. Inflammation in atherosclerosis: from pathophysiology to practice. J Am Coll Cardiol. 2009;54:2129-2138.
3. Erbay E, Babaev VR, Mayers JR, et al. Reducing endoplasmic reticulum stress through a macrophage lipid chaperone alleviates atherosclerosis. Nat Med. 2009;15:1383-1391.
4. Tabas I. The role of endoplasmic reticulum stress in the progression of atherosclerosis. Circ Res. 2010;107:839-850.
5. Luczak MW, Jagodzinski PP. The role of DNA methylation in cancer development. Folia Histochem Cytobiol. 2006;44:143-154.
6. Stenvinkel P, Karimi M, Johansson S, et al. Impact of inflammation on epigenetic DNA methylation - a novel risk factor for cardiovascular disease? J Intern Med. 2007;261:488-499.
7. Sharma P, Kumar J, Garg G, et al. Detection of altered global DNA methylation in coronary artery disease patients. DNA Cell Biol. 2008;27:357-365.
8. Dong C,Yoon W,Goldschmidt-Clermont PJ. DNA methylation and atherosclerosis. J Nutr. 2002;132:2406S-2409S.
9. Christman JK. 5-Azacytidine and 5-aza-2'-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Oncogene. 2002;21:5483-5495.
10. Patra SK, Bettuzzi S. Epigenetic DNA-(cytosine-5-carbon) modifications: 5-aza-2'-deoxycytidine and DNA-demethylation. Biochemistry (Mosc). 2009;74:613-619.
11. Stresemann C, Lyko F. Modes of action of the DNA methyltransferase inhibitors azacytidine and decitabine. Int J Cancer. 2008;123:8-13.
12. Li Q, Bartlett DL, Gorry MC, O'Malley ME, Guo ZS. Three epigenetic drugs up-regulate homeobox gene Rhox5 in cancer cells through overlapping and distinct molecular mechanisms. Mol Pharmacol. 2009;76:1072-1081.
13. Calkin AC, Tontonoz P. Liver X receptor signaling pathways and atherosclerosis. Arterioscler Thromb Vasc Biol. 2010;30:1513-1518.
14. Joseph SB, Castrillo A, Laffitte BA, Mangelsdorf DJ, Tontonoz P. Reciprocal regulation of inflammation and lipid metabolism by liver X receptors. Nat Med. 2003;9:213-219.
15. Gerry JM, Pascual G. Narrowing in on cardiovascular disease: the atheroprotective role of peroxisome proliferator-activated receptor gamma. Trends Cardiovasc Med. 2008;18:39-44.
16. Ishibashi S, Brown MS, Goldstein JL, Gerard RD, Hammer RE, Herz J. Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J Clin Invest. 1993;92:883-893.
17. Temel RE, Lee RG, Kelley KL, et al. Intestinal cholesterol absorption is substantially reduced in mice deficient in both ABCA1 and ACAT2. J Lipid Res. 2005;46:2423-2431.
18. Rong S, Cao Q, Liu M, et al. Macrophage 12/15 lipoxygenase expression increases plasma and hepatic lipid levels and exacerbates atherosclerosis. J Lipid Res. 2012;53:686-695.
19. Brown AL, Zhu X, Rong S, et al. Omega-3 fatty acids ameliorate atherosclerosis by favorably altering monocyte subsets and limiting monocyte recruitment to aortic lesions. Arterioscler Thromb Vasc Biol. 2012;32:2122-2130.
20. Galkina E, Kadl A, Sanders J, Varughese D, Sarembock IJ, Ley K. Lymphocyte recruitment into the aortic wall before and during development of atherosclerosis is partially L-selectin dependent. J Exp Med. 2006;203:1273-1282.
21. Wang X, Yang Z, Xue B, Shi H. Activation of the cholinergic antiinflammatory pathway ameliorates obesity-induced inflammation and insulin resistance. Endocrinology. 152:836-846.
22. Yang X, Wang X, Liu D, Yu L, Xue B, Shi H. Epigenetic regulation of macrophage polarization by DNAmethyltransferase 3b. Mol Endocrinol. 2014;28:565-574.
23. Zhu X, Lee JY, Timmins JM, et al. Increased cellular free cholesterol in macrophage-specific Abca1 knock-out mice enhances pro-inflammatory response of macrophages. J Biol Chem. 2008;283: 22930-22941.
24. Furbee JW Jr, Sawyer JK, Parks JS. Lecithin:cholesterol acyltransferase deficiency increases atherosclerosis in the low density lipoprotein receptor and apolipoprotein E knockout mice. J Biol Chem. 2002;277:3511-3519.
25. Fujiki K, Kano F, Shiota K, Murata M. Expression of the peroxisome proliferator activated receptor gamma gene is repressed by DNA methylation in visceral adipose tissue of mouse models of diabetes. BMC Biol. 2009;7:38.
26. Shore A, Karamitri A, Kemp P, Speakman JR, Lomax MA. Role of Ucp1 enhancer methylation and chromatin remodelling in the control of Ucp1 expression in murine adipose tissue. Diabetologia. 2010;53:1164-1173.
27. McCabe MT, Low JA, Daignault S, Imperiale MJ, Wojno KJ, Day ML. Inhibition of DNA methyltransferase activity prevents tumorigenesis in a mouse model of prostate cancer. Cancer Res. 2006;66:385-392.
28. Lusis AJ. Atherosclerosis. Nature. 2000;407:233-241.
29. Clozel T, Yang S, Elstrom RL, et al. Mechanism-based epigenetic chemosensitization therapy of diffuse large B-cell lymphoma. Cancer Discov. 2013;3:1002-1019.
30. Kalac M, Scotto L, Marchi E, et al. HDACinhibitors and decitabine are highly synergistic and associated with unique gene-expression and epigenetic profiles in models of DLBCL. Blood. 2011;118:5506-5516.
31. Hassler MR, Klisaroska A, Kollmann K, et al. Antineoplastic activity of the DNA methyltransferase inhibitor 5-aza-2'-deoxycytidine in anaplastic large cell lymphoma. Biochimie. 2012;94:2297-2307.
32. Gordon S, Hamann J, Lin HH, Stacey M. F4/80 and the related adhesion-GPCRs. Euro J Immunol. 2011;41:2472-2476.
33. Rosas M, Thomas B, Stacey M, Gordon S, Taylor PR. The myeloid 7/4-antigen defines recently generated inflammatory macrophages and is synonymous with Ly-6B. J Leukoc Biol. 2010;88:169-180.
34. Swirski FK, Libby P, Aikawa E, et al. Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest. 2007;117:195-205.
35. Perry HM, Bender TP, McNamara CA. B cell subsets in atherosclerosis. Front Immunol. 2012;3:373.
36. Creusot F, Acs G, Christman JK. Inhibition of DNA methyltransferase and induction of Friend erythroleukemia cell differentiation by 5-azacytidine and 5-aza-2'-deoxycytidine. J Biol Chem. 1982;257:2041-2048.
37. Tabas I. Macrophage apoptosis in atherosclerosis: consequences on plaque progression and the role of endoplasmic reticulum stress. Antioxid Redox Signal. 2009;11:2333-2339.
38. Bensinger SJ, Tontonoz P. Integration of metabolism and inflammation by lipid-activated nuclear receptors. Nature. 2008;454:470-477.
39. Babaev VR, Yancey PG, Ryzhov SV, et al. Conditional knockout of macrophage PPARgamma increases atherosclerosis in C57BL/6 and low-density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol. 2005;25:1647-1653.
40. Pascual G, Sullivan AL, Ogawa S, et al. Anti-inflammatory and antidiabetic roles of PPARgamma. Novartis Found Symp. 2007;286:183-196; discussion 196-203.
41. Staels B. PPARγ and atherosclerosis. Curr Med Res Opin. 2005;21(Suppl 1):S13-S20.
42. Tontonoz P, Hu E, Graves RA, Budavari AI, Spiegelman BM. mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev. 1994;8:1224-1234.
43. Zhu Y, Alvares K, Huang Q, Rao MS, Reddy JK. Cloning of a new member of the peroxisome proliferator-activated receptor gene family from mouse liver. J Biol Chem. 1993;268:26817-26820.
44. Zhu Y, Qi C, Korenberg JR, et al. Structural organization of mouse peroxisome proliferator-activated receptor gamma (mPPAR gamma) gene: alternative promoter use and different splicing yield two mPPAR gamma isoforms. Proc Natl Acad Sci U S A. 1995;92:7921-7925.
45. Lefterova MI, Steger DJ, Zhuo D, et al. Cell-specific determinants of peroxisome proliferator-activated receptor gamma function in adipocytes and macrophages. Mol Cell Biol. 2010;30:2078-2089.
46. Edwards TM, Myers JP. Environmental exposures and gene regulation in disease etiology. Environ Health Perspect. 2007;115:1264-1270.
47. Skinner MK, Manikkam M, Guerrero-Bosagna C. Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab. 2010;21:214-222.
48. Dunn J, Qiu H, Kim S, et al. Flow-dependent epigenetic DNA methylation regulates endothelial gene expression and atherosclerosis. J Clin Invest. 2014;124:3187-3199.
49. Lal G, Zhang N, van der Touw W, et al. Epigenetic regulation of Foxp3 expression in regulatory T cells by DNA methylation. J Immunol. 2009;182:259-273.
50. Lü CX, Xu RD, Cao M, et al. FOXP3 demethylation as a means of identifying quantitative defects in regulatory T cells in acute coronary syndrome. Atherosclerosis. 2013;229:263-270.
51. Sasaki N, Yamashita T, Takeda M, Hirata K. Regulatory T cells in atherogenesis. J Atheroscler Thromb. 2012;19:503-515.
52. Repa JJ, Mangelsdorf DJ. The liver X receptor gene team: potential new players in atherosclerosis. Nat Med. 2002;8:1243-1248.
53. de Winther MP, Kanters E, Kraal G, Hofker MH. Nuclear factor kappaB signaling in atherogenesis. Arterioscler Thromb Vasc Biol. 2005;25:904-914.
54. Odegaard JI, Ricardo-Gonzalez RR, Goforth MH, et al. Macro-phage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature. 2007;447:1116-1120.
55. Fabre C, Grosjean J, Tailler M, et al. A novel effect of DNA methyltransferase and histone deacetylase inhibitors: NFkappaB inhibition in malignant myeloblasts. Cell Cycle. 2008;7:2139-2145.
56. Wang J, Yang B, Han L, et al. Demethylation of miR-9-3 and miR-193a genes suppresses proliferation and promotes apoptosis in nonsmall cell lung cancer cell lines. Cell Physiol Biochem. 2013;32:1707-1719.
57. Jiang R, Li Y, Zhang A, et al. The acquisition of cancer stem cell-like properties and neoplastic transformation of human keratinocytes induced by arsenite involves epigenetic silencing of let-7c via Ras/NF-κB. Toxicol Lett. 2014;227:91-98.
58. Nguyen MT, Chen A, Lu WJ, et al. Regulation of chemokine and chemokine receptor expression by PPARgamma in adipocytes and macrophages. PLoS One. 2012;7:e34976.
59. Yoshiuchi K, Kaneto H, Matsuoka TA, et al. Pioglitazone reduces ER stress in the liver: direct monitoring of in vivo ER stress using ER stress-activated indicator transgenic mice. Endocr J. 2009;56:1103-1111.
60. Rong X, Albert CJ, Hong C, et al. LXRs regulate ER stress and inflammation through dynamic modulation of membrane phospholipid composition. Cell Metab. 2013;18:685-697.