SuperTAG methylation-specific digital karyotyping reveals uremia-induced epigenetic dysregulation of atherosclerosis-related genes

Circulation: Cardiovascular Genetics

Volumn 5, Issue 6, 2012, Pages 611-620

  Zawada, Adam M ^a   Rogacev, Kyrill S ^a   Hummel, Bj̈rn ^a   Grün, Oliver S ^a   Friedrich, Annika ^a   Rotter, Bj̈rn ^a,b   Winter, Peter ^a,b   Geisel, Jürgen ^a   Fliser, Danilo ^a   Heine, Gunnar H ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b GENXPRO GMBH   (Germany)

Author keywords

Cardiovascular diseases; DNA methylation; Epigenetics; Genome wide analysis; Kidney

Indexed keywords

ADULT; ARTICLE; ATHEROSCLEROSIS; CELL CYCLE REGULATION; CELL PROLIFERATION; CHRONIC KIDNEY DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; FEMALE; GENETIC ASSOCIATION; HEMODIALYSIS; HUMAN; KARYOTYPING; LIPID METABOLISM; MALE; METHYLATION SPECIFIC DIGITAL KARYOTYPING; PRIORITY JOURNAL; PROMOTER REGION; UREMIA;

ATHEROSCLEROSIS; CASE-CONTROL STUDIES; DATABASES, GENETIC; DNA METHYLATION; EPIGENESIS, GENETIC; HUMANS; KARYOTYPING; MALE; MIDDLE AGED; RENAL DIALYSIS; REPRODUCIBILITY OF RESULTS; S-ADENOSYLHOMOCYSTEINE; S-ADENOSYLMETHIONINE; UREMIA;

EID: 84873910693     PISSN: 1942325X     EISSN: 19423268     Source Type: Journal    
DOI: 10.1161/CIRCGENETICS.112.963207     Document Type: Article

References (50)

1. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med. 2004;351:1296-1305.
2. Sarnak MJ, Levey AS, Schoolwerth AC, Coresh J, Culleton B, Hamm LL, et al. Kidney disease as a risk factor for development of cardiovascular disease: A statement from the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Circulation. 2003;108:2154-2169.
3. Dwivedi RS, Herman JG, McCaffrey TA, Raj DS. Beyond genetics: Epigenetic code in chronic kidney disease. Kidney Int. 2011;79:23-32.
4. Ekström TJ, Stenvinkel P. The epigenetic conductor: A genomic orchestrator in chronic kidney disease complications? J Nephrol.2009;22:442-449.
5. Ingrosso D, Perna AF. Epigenetics in hyperhomocysteinemic states. A special focus on uremia. Biochim Biophys Acta. 2009;1790:892-899.
6. Perna AF, Ingrosso D, Violetti E, Luciano MG, Sepe I, Lanza D, et al. Hyperhomocysteinemia in uremia-a red flag in a disrupted circuit. Semin Dial. 2009;22:351-356.
7. Stenvinkel P, Ekström TJ. Epigenetics and the uremic phenotype: A matter of balance. Contrib Nephrol. 2008;161:55-62.
8. Stenvinkel P, Ekström TJ. Epigenetics-a helpful tool to better understand processes in clinical nephrology? Nephrol Dial Transplant. 2008;23:1493-1496.
9. Richards EJ. Inherited epigenetic variation-revisiting soft inheritance. Nat Rev Genet. 2006;7:395-401.
10. Geisel J, Schorr H, Heine GH, Bodis M, Hübner U, Knapp JP, et al. Decreased p66Shc promoter methylation in patients with end-stage renal disease. Clin Chem Lab Med. 2007;45:1764-1770.
11. Ingrosso D, Cimmino A, Perna AF, Masella L, De Santo NG, De Bonis ML, et al. Folate treatment and unbalanced methylation and changes of allelic expression induced by hyperhomocysteinaemia in patients with uraemia. Lancet. 2003;361:1693-1699.
12. Loehrer FM, Angst CP, Brunner FP, Haefeli WE, Fowler B. Evidence for disturbed S-adenosylmethionine: S-adenosylhomocysteine ratio in patients with end-stage renal failure: A cause for disturbed methylation reactions? Nephrol Dial Transplant. 1998;13:656-661.
13. Stenvinkel P, Karimi M, Johansson S, Axelsson J, Suliman M, Lindholm B, et al. Impact of inflammation on epigenetic DNA methylation-a novel risk factor for cardiovascular disease? J Intern Med. 2007;261:488-499.
14. Lund G, Andersson L, Lauria M, Lindholm M, Fraga MF, Villar-Garea A, et al. DNA methylation polymorphisms precede any histological sign of atherosclerosis in mice lacking apolipoprotein E. J Biol Chem. 2004;279:29147-29154.
15. Zaina S, Lindholm MW, Lund G. Nutrition and aberrant DNA methylation patterns in atherosclerosis: More than just hyperhomocysteinemia? J Nutr. 2005;135:5-8.
16. Valinluck V, Tsai HH, Rogstad DK, Burdzy A, Bird A, Sowers LC. Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res. 2004;32:4100-4108.
17. Bjornsson HT, Fallin MD, Feinberg AP. An integrated epigenetic and genetic approach to common human disease. Trends Genet. 2004;20:350-358.
18. Sapienza C, Lee J, Powell J, Erinle O, Yafai F, Reichert J, et al. DNA methylation profiling identifies epigenetic differences between diabetes patients with ESRD and diabetes patients without nephropathy. Epigenetics. 2011;6:20-28.
19. Hu M, Yao J, Cai L, Bachman KE, van den Brûle F, Velculescu V, et al. Distinct epigenetic changes in the stromal cells of breast cancers. Nat Genet. 2005;37:899-905.
20. Li J, Gao F, Li N, Li S, Yin G, Tian G, et al. An improved method for genome wide DNA methylation profiling correlated to transcription and genomic instability in two breast cancer cell lines. BMC Genomics. 2009;10:223.
21. Zawada AM, Rogacev KS, Rotter B, Winter P, Marell RR, Fliser D, et al. SuperSAGE evidence for CD14++CD16+ monocytes as a third monocyte subset. Blood. 2011;118:e50-e61.
22. Kirsch SH, Knapp JP, Geisel J, Herrmann W, Obeid R. Simultaneous quantification of S-adenosyl methionine and S-adenosyl homocysteine in human plasma by stable-isotope dilution ultra performance liquid chromatography tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci. 2009;877:3865-3870.
23. Matsumura H, Yoshida K, Luo S, Kimura E, Fujibe T, Albertyn Z, et al. High-throughput SuperSAGE for digital gene expression analysis of multiple samples using next generation sequencing. PLoS ONE. 2010;5:e12010.
24. Qu W, Hashimoto S, Morishita S. Efficient frequency-based de novo short-read clustering for error trimming in next-generation sequencing. Genome Res. 2009;19:1309-1315.
25. Audic S, Claverie JM. The significance of digital gene expression profiles. Genome Res. 1997;7:986-995.
26. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37:1-13.
27. Molina C, Rotter B, Horres R, Udupa SM, Besser B, Bellarmino L, et al. SuperSAGE: The drought stress-responsive transcriptome of chickpea roots. BMC Genomics. 2008;9:553.
28. Turunen MP, Aavik E, Ylä-Herttuala S. Epigenetics and atherosclerosis. Biochim Biophys Acta. 2009;1790:886-891.
29. Castro R, Rivera I, Struys EA, Jansen EE, Ravasco P, Camilo ME, et al. Increased homocysteine and S-adenosylhomocysteine concentrations and DNA hypomethylation in vascular disease. Clin Chem. 2003;49:1292-1296.
30. Guo Z, Ran Q, Roberts LJ 2nd, Zhou L, Richardson A, Sharan C, et al. Suppression of atherogenesis by overexpression of glutathione peroxidase-4 in apolipoprotein E-deficient mice. Free Radic Biol Med. 2008;44:343-352.
31. Ma L, Zhong J, Zhao Z, Luo Z, Ma S, Sun J, et al. Activation of TRPV1 reduces vascular lipid accumulation and attenuates atherosclerosis. Cardiovasc Res. 2011;92:504-513.
32. Rakyan VK, Down TA, Thorne NP, Flicek P, Kulesha E, Gräf S, et al. An integrated resource for genome-wide identification and analysis of human tissue-specific differentially methylated regions (tDMRs). Genome Res. 2008;18:1518-1529.
33. Perna AF, Capasso R, Lombardi C, Acanfora F, Satta E, Ingrosso D. Hyperhomocysteinemia and macromolecule modifications in uremic patients. Clin Chem Lab Med. 2005;43:1032-1038.
34. Mallamaci F, Zoccali C, Tripepi G, Fermo I, Benedetto FA, Cataliotti A, et al. Hyperhomocysteinemia predicts cardiovascular outcomes in hemodialysis patients. Kidney Int. 2002;61:609-614.
35. Bostom AG, Carpenter MA, Kusek JW, Levey AS, Hunsicker L, Pfeffer MA, et al. Homocysteine-lowering and cardiovascular disease outcomes in kidney transplant recipients: Primary results from the Folic Acid for Vascular Outcome Reduction in Transplantation trial. Circulation. 2011;123:1763-1770.
36. Heinz J, Kropf S, Domröse U, Westphal S, Borucki K, Luley C, et al. B vitamins and the risk of total mortality and cardiovascular disease in end-stage renal disease: Results of a randomized controlled trial. Circulation. 2010;121:1432-1438.
37. Jamison RL, Hartigan P, Kaufman JS, Goldfarb DS, Warren SR, Guarino PD, et al. Effect of homocysteine lowering on mortality and vascular disease in advanced chronic kidney disease and end-stage renal disease: A randomized controlled trial. JAMA. 2007;298:1163-1170.
38. Wrone EM, Hornberger JM, Zehnder JL, McCann LM, Coplon NS, Fortmann SP. Randomized trial of folic acid for prevention of cardiovascular events in end-stage renal disease. J Am Soc Nephrol. 2004;15:420-426.
39. Zoungas S, McGrath BP, Branley P, Kerr PG, Muske C, Wolfe R, et al. Cardiovascular morbidity and mortality in the Atherosclerosis and Folic Acid Supplementation Trial (ASFAST) in chronic renal failure: A multicenter, randomized, controlled trial. J Am Coll Cardiol. 2006;47:1108-1116.
40. Bazzano LA, Reynolds K, Holder KN, He J. Effect of folic acid supplementation on risk of cardiovascular diseases: A meta-analysis of randomized controlled trials. JAMA. 2006;296:2720-2726.
41. Lonn E, Yusuf S, Arnold MJ, Sheridan P, Pogue J, Micks M, et al. Homocysteine lowering with folic acid and B vitamins in vascular disease. N Engl J Med. 2006;354:1567-1577.
42. Liu C, Wang Q, Guo H, Xia M, Yuan Q, Hu Y, et al. Plasma S-adenosylhomocysteine is a better biomarker of atherosclerosis than homocysteine in apolipoprotein E-deficient mice fed high dietary methionine. J Nutr. 2008;138:311-315.
43. Valli A, Carrero JJ, Qureshi AR, Garibotto G, Bárány P, Axelsson J, et al. Elevated serum levels of S-adenosylhomocysteine, but not homocysteine, are associated with cardiovascular disease in stage 5 chronic kidney disease patients. Clin Chim Acta. 2008;395:106-110.
44. Green TJ, Skeaff CM, McMahon JA, Venn BJ, Williams SM, Devlin AM, et al. Homocysteine-lowering vitamins do not lower plasma S-adenosylhomocysteine in older people with elevated homocysteine concentrations. Br J Nutr. 2010;103:1629-1634.
45. Garibotto G, Valli A, Anderstam B, Eriksson M, Suliman ME, Balbi M, et al. The kidney is the major site of S-adenosylhomocysteine disposal in humans. Kidney Int. 2009;76:293-296.
46. Miyamoto T, Carrero JJ, Stenvinkel P. Inflammation as a risk factor and target for therapy in chronic kidney disease. Curr Opin Nephrol Hypertens. 2011;20:662-668.
47. Hodge DR, Xiao W, Clausen PA, Heidecker G, Szyf M, Farrar WL. Interleukin-6 regulation of the human DNA methyltransferase (HDNMT) gene in human erythroleukemia cells. J Biol Chem. 2001;276:39508-39511.
48. Fellstrom BC, Jardine AG, Schmieder RE, Holdaas H, Bannister K, Beutler J, et al. Rosuvastatin and cardiovascular events in patients undergoing hemodialysis. N Engl J Med. 2009;360:1395-1407.
49. Wanner C, Krane V, Marz W, Olschewski M, Mann JF, Ruf G, et al. Atorvastatin in patients with type 2 diabetes mellitus undergoing hemodialysis. N Engl J Med. 2005;353:238-248.
50. Zannad F, Kessler M, Lehert P, Grünfeld JP, Thuilliez C, Leizorovicz A, et al. Prevention of cardiovascular events in end-stage renal disease: Results of a randomized trial of fosinopril and implications for future studies. Kidney Int. 2006;70:1318-1324.