Identification and systematic annotation of tissue-specific differentially methylated regions using the Illumina 450k array

Epigenetics and Chromatin

Volumn 6, Issue 1, 2013, Pages

  Slieker, Roderick C ^a   Bos, Steffan D ^a,b   Goeman, Jelle J ^a   Bovée, Judith Vmg ^a   Talens, Rudolf P ^a   Van Der Breggen, Ruud ^a   Suchiman, H Eka D ^a   Lameijer, Eric Wubbo ^a   Putter, Hein ^a   Van Den Akker, Erik B ^a,c   Zhang, Yanju ^a   Jukema, J Wouter ^a   Slagboom, P Eline ^a,b   Meulenbelt, Ingrid ^a,b   Heijmans, Bastiaan T ^a,b  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Netherlands Center for Healthy Ageing   (Netherlands)

^c DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

Algorithm; Annotation; Differentially methylated region; Illumina 450k; Tissue

Indexed keywords

DEOXYRIBONUCLEASE; DNA; TRANSCRIPTION FACTOR;

ALGORITHM; ARTICLE; BINDING SITE; BLOOD; CHEEK; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EXON; GENETIC TRANSCRIPTION; HAIR FOLLICLE; LIVER; MUSCLE; OMENTUM; PANCREAS; PRIORITY JOURNAL; PROMOTER REGION; SALIVA; SPLEEN; SUBCUTANEOUS FAT; TISSUE SPECIFICITY; TRANSCRIPTION INITIATION SITE;

EID: 84881063347     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/1756-8935-6-26     Document Type: Article

References (51)

1. Programming of DNA methylation patterns. Cedar H, Bergman Y, Annu Rev Biochem 2012 81 97 117 10.1146/annurev-biochem-052610-091920 22404632
2. Epigenetic profiling of somatic tissues from human autopsy specimens identifies tissue-and individual-specific DNA methylation patterns. Byun HM, Siegmund KD, Pan F, Weisenberger DJ, Kanel G, Laird PW, Yang AS, Hum Mol Genet 2009 18 4808 4817 10.1093/hmg/ddp445 19776032
3. An integrated resource for genome-wide identification and analysis of human tissue-specific differentially methylated regions (tDMRs). Rakyan VK, Down TA, Thorne NP, Flicek P, Kulesha E, Graf S, Tomazou EM, Backdahl L, Johnson N, Herberth M, et al. Genome Res 2008 18 1518 1529 10.1101/gr.077479.108 18577705
4. A novel CpG island set identifies tissue-specific methylation at developmental gene loci. Illingworth R, Kerr A, Desousa D, Jorgensen H, Ellis P, Stalker J, Jackson D, Clee C, Plumb R, Rogers J, et al. PLoS Biol 2008 6 22 10.1371/journal.pbio.0060022 18232738 (Pubitemid 351226045)
5. Tissue specific differentially methylated regions (TDMR): changes in DNA methylation during development. Song F, Mahmood S, Ghosh S, Liang P, Smiraglia DJ, Nagase H, Held WA, Genomics 2009 93 130 139 10.1016/j.ygeno.2008.09.003 18952162
6. Dynamic changes in the human methylome during differentiation. Laurent L, Wong E, Li G, Huynh T, Tsirigos A, Ong CT, Low HM, Sung KWK, Rigoutsos I, Loring J, Genome Res 2010 20 320 331 10.1101/gr.101907.109 20133333
7. Tissue-specific demethylation in CpG-poor promoters during cellular differentiation. Nagae G, Isagawa T, Shiraki N, Fujita T, Yamamoto S, Tsutsumi S, Nonaka A, Yoshiba S, Matsusaka K, Midorikawa Y, Hum Mol Genet 2011 20 2710 2721 10.1093/hmg/ddr170 21505077
8. CpG methylation recruits sequence specific transcription factors essential for tissue specific gene expression. Chatterjee R, Vinson C, Biochim Biophy Acta (BBA)-Gene Regul Mechan 2012 1819 763 770 10.1016/j.bbagrm.2012.02. 014 849477
9. Cell type-specific DNA methylation at intragenic CpG islands in the immune system. Deaton AM, Webb S, Kerr AR, Illingworth RS, Guy J, Andrews R, Bird A, Genome Res 2011 21 1074 1086 10.1101/gr.118703.110 21628449
10. Conserved role of intragenic DNA methylation in regulating alternative promoters. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C, Fouse SD, Johnson BE, Hong C, Nielsen C, Zhao Y, Nature 2010 466 253 257 10.1038/nature09165 20613842
11. Functional annotation of the human brain methylome identifies tissue-specific epigenetic variation across brain and blood. Davies M, Volta M, Pidsley R, Lunnon K, Dixit A, Lovestone S, Coarfa C, Harris RA, Milosavljevic A, Troakes C, Genome Biol 2012 13 43 10.1186/gb-2012-13-6-r43 22703893
12. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M, Nat Genet 2009 41 178 186 10.1038/ng.298 19151715
13. Variation, patterns, and temporal stability of DNA methylation: considerations for epigenetic epidemiology. Talens RP, Boomsma DI, Tobi EW, Kremer D, Jukema JW, Willemsen G, Putter H, Slagboom PE, Heijmans BT, FASEB J 2010 24 3135 3144 10.1096/fj.09-150490 20385621
14. Evaluation of the Infinium Methylation 450K technology. Dedeurwaerder S, Defrance M, Calonne E, Denis H, Sotiriou C, Fuks F, Epigenomics 2011 3 771 784 10.2217/epi.11.105 22126295
15. Quantitative cross-validation and content analysis of the 450k DNA methylation array from Illumina. Roessler J, Ammerpohl O, Gutwein J, Hasemeier B, Anwar SL, Kreipe H, Lehmann U, Inc BMC Res Notes 2012 5 210 10.1186/1756-0500-5-210
16. Buccal swabs but not mouthwash samples can be used to obtain pretransplant DNA fingerprints from recipients of allogeneic bone marrow transplants. Thiede C, Prange-Krex G, Freiberg-Richter J, Bornhäuser M, Ehninger G, Bone Marrow Transplant 2000 25 575 10713640
17. TiGER: a database for tissue-specific gene expression and regulation. Liu X, Yu X, Zack DJ, Zhu H, Qian J, BMC Bioinforma 2008 9 271 10.1186/1471-2105-9- 271 (Pubitemid 351895528)
18. DNA methylation signatures in development and aging of the human prefrontal cortex. Numata S, Ye T, Hyde TM, Guitart-Navarro X, Tao R, Wininger M, Colantuoni C, Weinberger DR, Kleinman JE, Lipska BK, Am J Hum Genet 2012 90 260 272 10.1016/j.ajhg.2011.12.020 22305529
19. Systematic localization of common disease-associated variation in regulatory DNA. Maurano MT, Humbert R, Rynes E, Thurman RE, Haugen E, Wang H, Reynolds AP, Sandstrom R, Qu H, Brody J, et al. Science 2012 337 1190 1195 10.1126/science.1222794 22955828
20. An integrated encyclopedia of DNA elements in the human genome. The ENCODE project Consortium, Nature 2012 489 57 74 10.1038/nature11247 22955616
21. Docosahexaenoic acid suppresses apolipoprotein A-I gene expression through hepatocyte nuclear factor-3ß Kuang YL, Paulson KE, Lichtenstein AH, Matthan NR, Lamon-Fava S, Am J Clin Nutr 2011 94 594 600 10.3945/ajcn.111.012526 21653803
22. Dynamic regulation of Pdx1 enhancers by Foxa1 and Foxa2 is essential for pancreas development. Gao N, LeLay J, Vatamaniuk MZ, Rieck S, Friedman JR, Kaestner KH, Genes Dev 2008 22 3435 3448 10.1101/gad.1752608 19141476
23. Male-pattern baldness susceptibility locus at 20p11. Richards JB, Yuan X, Geller F, Waterworth D, Bataille V, Glass D, Song K, Waeber G, Vollenweider P, Aben KKH, Nat Genet 2008 40 1282 1284 10.1038/ng.255 18849991
24. DNA methylation profile of tissue-dependent and differentially methylated regions (T-DMRs) in mouse promoter regions demonstrating tissue-specific gene expression. Yagi S, Hirabayashi K, Sato S, Li W, Takahashi Y, Hirakawa T, Wu G, Hattori N, Hattori N, Ohgane J, Genome Res 2008 18 1969 1978 10.1101/gr.074070.107 18971312
25. Genome-wide survey reveals dynamic widespread tissue-specific changes in DNA methylation during development. Liang P, Song F, Ghosh S, Morien E, Qin M, Mahmood S, Fujiwara K, Igarashi J, Nagase H, Held WA, BMC Genomics 2011 12 231 10.1186/1471-2164-12-231 21569359
26. Epigenetic features are significantly associated with alternative splicing. Zhou Y, Lu Y, Tian W, BMC Genomics 2012 13 123 10.1186/1471-2164-13- 123 22455468
27. Genetics and epigenetics: stability and plasticity during cellular differentiation. Mohn F, Schübeler D, Trends Genet 2009 25 129 136 10.1016/j.tig.2008.12.005 19185382
28. Redefining CpG Islands using a hidden Markov model. Wu H, Caffo B, Jaffee HA, Feinberg AP, Irizarry RA, Biostatistics 2009 11 499 514
29. CG dinucleotide clustering is a species-specific property of the genome. Glass JL, Thompson RF, Khulan B, Figueroa ME, Olivier EN, Oakley EJ, Van Zant G, Bouhassira EE, Melnick A, Golden A, Nucleic Acids Res 2007 35 6798 6807 10.1093/nar/gkm489 17932072 (Pubitemid 350201800)
30. CpGcluster: a distance-based algorithm for CpG-island detection. Hackenberg M, Previti C, Luque-Escamilla PL, Carpena P, Martinez-Aroza J, Oliver JL, BMC Bioinforma 2006 7 446 10.1186/1471-2105-7-446 (Pubitemid 44614256)
31. The accessible chromatin landscape of the human genome. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, Sheffield NC, Stergachis AB, Wang H, Vernot B, Nature 2012 489 75 82 10.1038/nature11232 22955617
32. DNA-binding factors shape the mouse methylome at distal regulatory regions. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Schöler A, Wirbelauer C, Oakeley EJ, Gaidatzis D, Tiwari VK, Nature 2011 480 490 495 22170606
33. Commentary: the seven plagues of epigenetic epidemiology. Heijmans BT, Mill J, Int J Epidemiol 2012 41 74 78 10.1093/ije/dyr225 22269254
34. DNA methylation patterns associate with genetic and gene expression variation in HapMap cell lines. Bell JT, Pai AA, Pickrell JK, Gaffney DJ, Pique-Regi R, Degner JF, Gilad Y, Pritchard JK, Genome Biol 2011 12 10 10.1186/gb-2011-12-1-r10 21251332
35. The Genotype-Tissue Expression (GTEx) project. Lonsdale J, Thomas J, Salvatore M, Phillips R, Lo E, Shad S, Hasz R, Walters G, Garcia F, Young N, et al. Nat Genet 2013 45 580 585 10.1038/ng.2653 23715323
36. High microsatellite and SNP genotyping success rates established in a large number of genomic DNA samples extracted from mouth swabs and genotypes. Min JL, Lakenberg N, Bakker-Verweij M, Suchiman E, Boomsma DI, Slagboom PE, Meulenbelt I, Twin Res Hum Genet 2006 9 501 506 10.1375/twin.9.4.501 16899157 (Pubitemid 46381680)
37. Kasper Daniel Hansen and Martin Aryee, minfi: Analyze Illumina's 450k methylation arrays. R package version 1.6.0 Bioconductor 2012
38. Triche T Jr, IlluminaHumanMethylation450k.db: Illumina Human Methylation 450k annotation data. R package version 1.4.7 Bioconductor 2012
39. Bates D, Maechler M, Bolker B, lme4: Linear mixed-effects models using S4 classes Bioconductor 2012
40. The DNA methylome of human peripheral blood mononuclear cells. Li Y, Zhu J, Tian G, Li N, Li Q, Ye M, Zheng H, Yu J, Wu H, Sun J, PLoS Biol 2010 8 1000533 10.1371/journal.pbio.1000533 21085693
41. The human genome browser at UCSC. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D, Genome Res 2002 12 996 1006 http://genome.ucsc.edu 12045153 (Pubitemid 34662293)
42. Alternative isoform regulation in human tissue transcriptomes. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB, Nature 2008 456 470 476 10.1038/nature07509 18978772 (Pubitemid 352759009)
43. ASTD: the alternative splicing and transcript diversity database. Koscielny G, Texier VL, Gopalakrishnan C, Kumanduri V, Riethoven JJ, Nardone F, Stanley E, Fallsehr C, Hofmann O, Kull M, Genomics 2009 93 213 220 10.1016/j.ygeno.2008.11.003 19059335
44. Ensembl http://www.ensembl.org
45. GREAT improves functional interpretation of cis-regulatory regions. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G, Nat Biotechnol 2010 28 495 501 10.1038/nbt.1630 20436461
46. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Huang DW, Sherman BT, Lempicki RA, Nucleic Acids Res 2009 37 1 13 10.1093/nar/gkn923 19033363
47. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Huang DW, Sherman BT, Lempicki RA, Nat Protoc 2009 4 44 57 19131956
48. REVIGO summarizes and visualizes long lists of gene ontology terms. Supek F, Bosnjak M, Skunca N, Smuc T, PLoS One 2011 6 21800 10.1371/journal.pone. 0021800 21789182
49. Hahne F, Durinck S, Ivankek R, Mueller A, Lianoglou S, Gviz: Plotting data and annotation information along genomic coordinates. R package version 1.2.1 Bioconductor 2012
50. Wickham H, ggplot2: Elegant graphics for data analysis New York: Springer 2009
51. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Edgar R, Domrachev M, Lash AE, Nucleic Acids Res 2002 30 1 207 210 10.1093/nar/30.1.207 11752295 (Pubitemid 34679544)