Human native lipoprotein-induced de novo DNA methylation is associated with repression of inflammatory genes in THP-1 macrophages

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Rangel Salazar, Rubén ^a   Wickström Lindholm, Marie ^b   Aguilar Salinas, Carlos A ^c   Alvarado Caudillo, Yolanda ^a   Døssing, Kristina B V ^e   Esteller, Manel ^d   Labourier, Emmanuel ^f   Lund, Gertrud ^g   Nielsen, Finn C ^e   Rodríguez Ríos, Dalia ^g   Solís Martínez, Martha O ^a   Wrobel, Katarzyna ^a   Wrobel, Kazimierz ^a   Zaina, Silvio ^a,b,e  

^a UNIVERSITY OF GUANAJUATO   (Mexico)

^b LUND UNIVERSITY   (Sweden)

^c National Institute of Medical Science and Nutrition   (Mexico)

^d BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^e University of Copenhagen   (Denmark)

^f ASURAGEN INC   (United States)

^g DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 2; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; DNA METHYLTRANSFERASE 3L; LIPOPROTEIN; MICRORNA; UNCLASSIFIED DRUG; HISTONE;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; DEACETYLATION; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; GENE EXPRESSION REGULATION; GENE MAPPING; GENE REPRESSION; GENE TARGETING; HISTONE MODIFICATION; HUMAN; HUMAN CELL; MACROPHAGE; RNA INTERFERENCE; UPREGULATION; CELL LINE; GENE SILENCING; GENETIC EPIGENESIS; GENETICS; INFLAMMATION; METABOLISM; PROMOTER REGION; PROTEIN PROCESSING; PROTEOMICS;

MAMMALIA;

CELL LINE; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; GENE SILENCING; HISTONES; HUMANS; INFLAMMATION; LIPOPROTEINS; MACROPHAGES; MICRORNAS; PROMOTER REGIONS, GENETIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS;

EID: 82055171836     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-582     Document Type: Article

References (55)

1. Libby P, Theroux P. Pathophysiology of coronary artery disease. Circulation 2005, 111:3481-3488. 10.1161/CIRCULATIONAHA.105.537878, 15983262.
2. Ordovás JM, Smith CE. Epigenetics and cardiovascular disease. Nat Rev Cardiol 2010, 7:510-519. 10.1038/nrcardio.2010.104, 3075976, 20603647.
3. Waterland RA, Jirtle RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 2003, 23:5293-5300. 10.1128/MCB.23.15.5293-5300.2003, 165709, 12861015.
4. Gallou-Kabani C, Vigé A, Gross MS, Junien C. Nutri-epigenomics: lifelong remodelling of our epigenomes by nutritional and metabolic factors and beyond. Clin Chem Lab Med 2007, 45:321-327. 10.1515/CCLM.2007.081, 17378726.
5. Laukkanen MO, Mannermaa S, Hiltunen MO, Aittomäki S, Airenne K, Jänne J, Ylä-Herttuala S. Local hypomethylation in atherosclerosis found in rabbit ec-sod gene. Arterioscler Thromb Vasc Biol 1999, 19:2171-2178. 10.1161/01.ATV.19.9.2171, 10479660.
6. Hiltunen MO, Turunen MP, Häkkinen TP, Rutanen J, Hedman M, Mäkinen K, Turunen AM, Aalto-Setälä K, Ylä-Herttuala S. DNA hypomethylation and methyltransferase expression in atherosclerotic lesions. Vasc Med 2002, 7:5-11. 10.1191/1358863x02vm418oa, 12083735.
7. Lund G, Andersson L, Lauria M, Lindholm M, Fraga MF, Villar-Garea A, Ballestar E, Esteller M, Zaina S. DNA methylation polymorphisms precede any histological sign of atherosclerosis in mice lacking apolipoprotein E. J Biol Chem 2004, 279:29147-29154. 10.1074/jbc.M403618200, 15131116.
8. Huang Y, Peng K, Su J, Huang Y, Xu Y, Wang S. Different effects of homocysteine and oxidized low density lipoprotein on methylation status in the promoter region of the estrogen receptor alpha gene. Acta Biochim Biophys Sin (Shanghai) 2007, 39:19-26.
9. Chen KC, Wang YS, Hu CY, Chang WC, Liao YC, Dai CY, Juo SH. OxLDL up-regulates microRNA-29b, leading to epigenetic modifications of MMP-2/MMP-9 genes: a novel mechanism for cardiovascular diseases. FASEB J 2011, 25:1718-1728. 10.1096/fj.10-174904, 21266537.
10. Bauer S, Robinson PN, Gagneur J. Model-based gene set analysis for Bioconductor. Bioinformatics 2011, 27:1882-1883. 10.1093/bioinformatics/btr296, 3117381, 21561920.
11. Bauer S, Gagneur J, Robinson PN. GOing Bayesian: model-based gene set analysis of genome-scale data. Nucleic Acids Res 2010, 38:3523-3532. 10.1093/nar/gkq045, 2887944, 20172960.
12. Alcázar-Magaña A, Wrobel K, Alvarado-Caudillo Y, Zaina S, Lund G, Wrobel K. High performance liquid chromatography determination of 5-methyl-2'-deoxycytidine (5 mdC), 2'-deoxycytidine (dC) and other deoxynucleosides and nucleosides in DNA digests. Anal Biochem 2008, 374:378-385. 10.1016/j.ab.2007.11.026, 18157934.
13. Worm J, Aggerholm A, Guldberg P. In-tube DNA methylation profiling by fluorescence melting curve analysis. Clin Chem 2001, 47:1183-1189.
14. Schreiber E, Matthias P, Müller MM, Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res 1989, 17:6419. 10.1093/nar/17.15.6419, 318318, 2771659.
15. Shingara J, Keiger K, Shelton J, Laosinchai-Wolf W, Powers P, Conrad R, Brown D, Labourier E. An optimized isolation and labeling platform for accurate microRNA expression profiling. RNA 2005, 11:1461-1470. 10.1261/rna.2610405, 1370829, 16043497.
16. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 2006, 126:1189-1201. 10.1016/j.cell.2006.08.003, 16949657.
17. Rauch TA, Wu X, Zhong X, Riggs AD, Pfeifer GP. A human B cell methylome at 100-base pair resolution. Proc Natl Acad Sci USA 2009, 106:671-678. 10.1073/pnas.0812399106, 2621253, 19139413.
18. Muzio M, Ni J, Feng P, Dixit VM. IRAK (Pelle) family member IRAK-2 and MyD88 as proximal mediators of IL-1 signaling. Science 1997, 278:1612-1615. 10.1126/science.278.5343.1612, 9374458.
19. Breviario F, d'Aniello EM, Golay J, Peri G, Bottazzi B, Bairoch A, Saccone S, Marzella R, Predazzi V, Rocchi M. Interleukin-1-inducible genes in endothelial cells. Cloning of a new gene related to C-reactive protein and serum amyloid P component. J Biol Chem 1992, 267:22190-22197.
20. Rolph MS, Zimmer S, Bottazzi B, Garlanda C, Mantovani A, Hansson GK. Production of the long pentraxin PTX3 in advanced atherosclerotic plaques. Arterioscler Thromb Vasc Biol 2002, 22:e10-e14. 10.1161/01.ATV.0000015595.95497.2F, 12006411.
21. Zirlik A, Bavendiek U, Libby P, MacFarlane L, Gerdes N, Jagielska J, Ernst S, Aikawa M, Nakano H, Tsitsikov E, Schönbeck U. TRAF-1, -2, -3, -5, and -6 are induced in atherosclerotic plaques and differentially mediate proinflammatory functions of CD40L in endothelial cells. Arterioscler Thromb Vasc Biol 2007, 27:1101-1107. 10.1161/ATVBAHA.107.140566, 17332487.
22. Robert MF, Morin S, Beaulieu N, Gauthier F, Chute IC, Barsalou A, MacLeod AR. DNMT1 is required to maintain CpG methylation and aberrant gene silencing in human cancer cells. Nat Genet 2003, 33:61-65. 10.1038/ng1068, 12496760.
23. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999, 99:247-257. 10.1016/S0092-8674(00)81656-6, 10555141.
24. Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z, Erdjument-Bromage H, Tempst P, Lin SP, Allis CD, Cheng X, Bestor TH. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 2007, 448:714-717. 10.1038/nature05987, 2650820, 17687327.
25. Jeltsch A, Nellen W, Lyko F. Two substrates are better than one: dual specificities for Dnmt2 methyltransferases. Trends Biochem Sci 2006, 31:306-308. 10.1016/j.tibs.2006.04.005, 16679017.
26. Goll MG, Kirpekar F, Maggert KA, Yoder JA, Hsieh CL, Zhang X, Golic KG, Jacobsen SE, Bestor TH. Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 2006, 311:395-398. 10.1126/science.1120976, 16424344.
27. You JS, Kang JK, Lee EK, Lee JC, Lee SH, Jeon YJ, Koh DH, Ahn SH, Seo DW, Lee HY, Cho EJ, Han JW. Histone deacetylase inhibitor apicidin downregulates DNA methyltransferase 1 expression and induces repressive histone modifications via recruitment of corepressor complex to promoter region in human cervix cancer cells. Oncogene 2008, 27:1376-1386. 10.1038/sj.onc.1210776, 17828306.
28. Standaert ML, Bandyopadhyay G, Kanoh Y, Sajan MP, Farese RV. Insulin and PIP3 activate PKC-zeta by mechanisms that are both dependent and independent of phosphorylation of activation loop (T410) and autophosphorylation (T560) sites. Biochemistry 2001, 40:249-255. 10.1021/bi0018234, 11141077.
29. Fukagawa T, Nogami M, Yoshikawa M, Ikeno M, Okazaki T, Takami Y, Nakayama T, Oshimura M. Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat Cell Biol 2004, 6:784-791. 10.1038/ncb1155, 15247924.
30. Ting AH, Suzuki H, Cope L, Schuebel KE, Lee BH, Toyota M, Imai K, Shinomura Y, Tokino T, Baylin SB. A requirement for DICER to maintain full promoter CpG island hypermethylation in human cancer cells. Cancer Res 2008, 68:2570-2575. 10.1158/0008-5472.CAN-07-6405, 2828041, 18413723.
31. Grewal SIS, Elgin SCR. Transcription and RNA interference in the formation of heterochromatin. Nature 2007, 447:399-406. 10.1038/nature05914, 2950806, 17522672.
32. Guil S, Esteller E. DNA methylomes, histone codes and miRNAs: tying it all together. Int J Biochem Cell Biol 2009, 41:87-95. 10.1016/j.biocel.2008.09.005, 18834952.
33. Yeramian A, Martin L, Serrat N, Arpa L, Soler C, Bertran J, McLeod C, Palacín M, Modolell M, Lloberas J, Celada A. Arginine transport via cationic amino acid transporter 2 plays a critical regulatory role in classical or alternative activation of macrophages. J Immunol 2006, 176:5918-5924.
34. Libby P. Fat fuels the flame: triglyceride-rich lipoproteins and arterial inflammation. Circ Res 2007, 100:299-301. 10.1161/01.RES.0000259393.89870.58, 17307968.
35. Ting HJ, Stice JP, Schaff UY, Hui DY, Rutledge JC, Knowlton AA, Passerini AG, Simon SI. Triglyceride-rich lipoproteins prime aortic endothelium for an enhanced inflammatory response to tumor necrosis factor-alpha. Circ Res 2007, 100:381-390. 10.1161/01.RES.0000258023.76515.a3, 17234968.
36. Stollenwerk MM, Schiopu A, Fredrikson GN, Dichtl W, Nilsson J, Ares MP. Very low density lipoprotein potentiates tumor necrosis factor-alpha expression in macrophages. Atherosclerosis 2005, 179:247-254. 10.1016/j.atherosclerosis.2004.12.002, 15777538.
37. Persson J, Nilsson J, Lindholm MW. Cytokine response to lipoprotein lipid loading in human monocyte-derived macrophages. Lipids Health Dis 2006, 5:17. 10.1186/1476-511X-5-17, 1524960, 16800873.
38. Batt KV, Patel L, Botham KM, Suckling KE. Chylomicron remnants and oxidised low density lipoprotein have differential effects on the expression of mRNA for genes involved in human macrophage foam cell formation. J Mol Med 2004, 82:449-458.
39. Masters SL, Dunne A, Subramanian SL, Hull RL, Tannahill GM, Sharp FA, Becker C, Franchi L, Yoshihara E, Chen Z, Mullooly N, Mielke LA, Harris J, Coll RC, Mills KH, Mok KH, Newsholme P, Nuñez G, Yodoi J, Kahn SE, Lavelle EC, O'Neill LA. Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1β in type 2 diabetes. Nat Immunol 2010, 11:897-904. 10.1038/ni.1935, 3103663, 20835230.
40. Harris HW, Grunfeld C, Feingold KR, Rapp JH. Human very low density lipoproteins and chylomicrons can protect against endotoxin-induced death in mice. J Clin Invest 1990, 86:696-702. 10.1172/JCI114765, 296783, 2394827.
41. Keshet I, Schlesinger Y, Farkash S, Rand E, Hecht M, Segal E, Pikarski E, Young RA, Niveleau A, Cedar H, Simon I. Evidence for an instructive mechanism of de novo methylation in cancer cells. Nat Genet 2006, 38:149-153. 10.1038/ng1719, 16444255.
42. Stenvinkel P, Karimi M, Johansson S, Axelsson J, Suliman M, Lindholm B, Heimbürger O, Barany P, Alvestrand A, Nordfors L, Qureshi AR, Ekström TJ, Schalling M. Impact of inflammation on epigenetic DNA methylation - a novel risk factor for cardiovascular disease?. J Intern Med 2007, 261:488-499. 10.1111/j.1365-2796.2007.01777.x, 17444888.
43. Barrès R, Osler ME, Yan J, Rune A, Fritz T, Caidahl K, Krook A, Zierath JR. Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab 2009, 10:189-198. 10.1016/j.cmet.2009.07.011, 19723495.
44. Lavoie G, Esteve PO, Bibens-Laulan N, Predhan S, St-Pierre Y. PKC isoforms interact with and phosphorylate DNMT1. BMC Biol 2011, 9:31. 10.1186/1741-7007-9-31, 3118390, 21619587.
45. Liang G, Chan MF, Tomigahara Y, Tsai YC, Gonzales FA, Li E, Laird PW, Jones PA. Cooperativity between DNA methyltransferases in the maintenance methylation of repetitive elements. Mol Cell Biol 2002, 22:480-491. 10.1128/MCB.22.2.480-491.2002, 139739, 11756544.
46. Kim GD, Ni J, Kelesoglu N, Roberts RJ, Pradhan S. Co-operation and communication between the human maintenance and de novo DNA (cytosine-5) methyltransferases. EMBO J 2002, 21:4183-4195. 10.1093/emboj/cdf401, 126147, 12145218.
47. Choi SH, Heo K, Byun HM, An W, Lu W, Yang AS. Identification of preferential target sites for human DNA methyltransferases. Nucleic Acids Res 2011, 39:104-118. 10.1093/nar/gkq774, 3017615, 20841325.
48. Grandjean V, Yaman R, Cuzin F, Rassoulzadegan M. Inheritance of an epigenetic mark: the CpG DNA methyltransferase 1 is required for de novo establishment of a complex pattern of non-CpG methylation. PLoS One 2007, 2:e1136. 10.1371/journal.pone.0001136, 2065839, 17989773.
49. MacDonald JL, Gin CS, Roskams AJ. Stage-specific induction of DNA methyltransferases in olfactory receptor neuron development. Dev Biol 2005, 288:461-473. 10.1016/j.ydbio.2005.09.048, 16288735.
50. Mizuno S, Chijiwa T, Okamura T, Akashi K, Fukumaki Y, Niho Y, Sasaki H. Expression of DNA methyltransferases DNMT1, 3A, and 3B in normal hematopoiesis and in acute and chronic myelogenous leukemia. Blood 2001, 97:1172-1179. 10.1182/blood.V97.5.1172, 11222358.
51. Foran E, Garrity-Park MM, Mureau C, Newell J, Smyrk TC, Limburg PJ, Egan LJ. Upregulation of DNA methyltransferase-mediated gene silencing, anchorage-independent growth, and migration of colon cancer cells by interleukin-6. Mol Cancer Res 2010, 8:471-481. 10.1158/1541-7786.MCR-09-0496, 20354000.
52. Chen CC, Chen WC, Wang WH, Lu CH, Lin PY, Lee KD, Chen MF. Role of DNA methyltransferase 1 in pharyngeal cancer related to treatment resistance. Head Neck 2011,
53. Hodge DR, Cho E, Copeland TD, Guszczynski T, Yang E, Seth AK, Farrar WL. IL-6 enhances the nuclear translocation of DNA cytosine-5-methyltransferase 1 (DNMT1) via phosphorylation of the nuclear localization sequence by the AKT kinase. Cancer Genomics Proteomics 2007, 4:387-398.
54. Mosher RA, Schwach F, Studholme D, Baulcombe DC. PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc Natl Acad Sci USA 2008, 105:3145-3150. 10.1073/pnas.0709632105, 2268599, 18287047.
55. Balan V, Leicht DT, Zhu J, Balan K, Kaplun A, Singh-Gupta V, Qin J, Ruan H, Comb MJ, Tzivion G. Identification of novel in vivo Raf-1 phosphorylation sites mediating positive feedback Raf-1 regulation by extracellular signal-regulated kinase. Mol Biol Cell 2006, 17:1141-1153. 1382304, 16407412.