Whole-genome bisulfite sequencing of multiple individuals reveals complementary roles of promoter and gene body methylation in transcriptional regulation

Genome Biology

Volumn 15, Issue 7, 2014, Pages

  Lou, Shaoke ^a   Lee, Heung Man ^a   Qin, Hao ^a   Li, Jing Woei ^a   Gao, Zhibo ^b   Liu, Xin ^b   Chan, Landon L ^a   Lam, Vincent K L ^a   So, Wing Yee ^a   Wang, Ying ^a   Lok, Si ^a   Wang, Jun ^b,c,d,e   Ma, Ronald C W ^a   Tsui, Stephen Kwok Wing ^a   Chan, Juliana C N ^a   Chan, Ting Fung ^a   Yip, Kevin Y ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b BGI SHENZHEN   (China)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d University of Copenhagen   (Denmark)

^e KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

MELATONIN; METHYLTRANSFERASE;

ARTICLE; BISULFITE SEQUENCE; CPG ISLAND; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENE MAPPING; GENE SEQUENCE; HIGH THROUGHPUT SEQUENCING; HISTONE MODIFICATION; HUMAN; IMMUNOPRECIPITATION; PERIPHERAL BLOOD MONONUCLEAR CELL; PROMOTER REGION; RNA SEQUENCE; TRANSCRIPTION REGULATION; CELL LINE; DNA SEQUENCE; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMAN GENOME; MALE; MOLECULAR GENETICS; PROCEDURES; SEQUENCE ANALYSIS; STATISTICAL MODEL;

CELL LINE; DNA METHYLATION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME, HUMAN; HUMANS; MALE; MODELS, STATISTICAL; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, RNA;

EID: 84929628130     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-014-0408-0     Document Type: Article

References (66)

1. Bird A: DNAmethylation patterns and epigeneticmemory. Genes Dev 2002, 16:6-21.
2. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE: Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNAmethylation patterning. Nature 2008, 452:215-219.
3. Lister R, O'Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR: Highly integrated single-base resolutionmaps of the epigenome in Arabidopsis. Cell 2008, 133:523-536.
4. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo Q, Edsall L, Antosiewicz-Bourget J, Stewart R, Ruotti V, Millar AH, Thomson JA, Ren B, Ecker JR: Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009, 462:315-322.
5. Ehrlich M, Gama-Sosa MA, Huang LH, Midgett RM, Kuo KC, McCune RA, Gehrke C: Amount and distribution of 5-methylcytosine in human DNA from different types of tissues of cells. Nucleic Acids Res 1982, 10:2709-2721.
6. Bird AP: CpG-rich islands and the function of DNA methylation. Nature 1986, 321:209-213.
7. Miranda TB, Jones PA: DNAmethylation: the nuts and bolts of repression. J Cell Physiol 2007, 213:384-390.
8. Suzuki MM, Bird A: DNAmethylation landscapes: provocative insights from epigenomics. Nat Rev Genet 2008, 9:465-476.
9. Kass SU, Pruss D, Wolffe AP: How does DNAmethylation repress transcription. Trends Genet 1977, 13:444-449.
10. Robertson KD: DNAmethylation and human disease. Nat Rev Genet 2005, 6:597-610.
11. Portela A, Esteller M: Epigenetic modifications and human disease. Nat Biotechnol 2010, 28:1057-1068.
12. Beck S, Rakyan VK: Themethylome: approaches for global DNA methylation profiling. Trends Genet 2008, 24:231-237.
13. Laird PW: Principles and challenges of genomewide DNA methylation analysis. Nat Rev Genet 2010, 11:191-203.
14. Jones PA: Functions of DNAmethylation: islands start sites gene bodies and beyond. Nat Rev Genet 2012, 13:484-492.
15. Lippman Z, Gendrel A-V, Colot V, Martienssen R: Profiling DNA methylation patterns using genomic tiling microarrays. Nat Methods 2005, 2:219-224.
16. Khulan B, Thompson RF, Ye K, Fazzari MJ, Suzuki M, Stasiek E, Figueroa ME, Glass JL, Chen Q, Montagna C, Hatchwell E, Selzer RR, Richmond T, Green RD, Melnick A, Greally J: Comparative isoschizomer profiling of cytosine methylation: the HELP assay. Genome Res 2006, 16:1046-1055.
17. Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL, Schübeler D: Chromosome-wide and promoter-specific analyses identify sites of differential DNAmethylation in normal and transformed human cells. Nat Genet 2005, 37:853-862.
18. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan S. W-L, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE: Genome-wide high-resolutionmapping and functional analysis of DNA methylation in Arabidopsis. Cell 2006, 126:1189-1201.
19. Weber M, Hellmann I, Stadler MB, Ramos L, Pääbo S, Rebhan M, Schübeler D: Distribution silencing potential and evolutionary impact of promoter DNAmethylation in the human genome. Nat Genet 2007, 39:457-466.
20. Illingworth R, Kerr A, Desousa D, Jørgensen H, Ellis P, Stalker J, Jackson D, Clee C, Plumb R, Rogers J, Humphray S, Cox T, Langford C, Bird A: A novel CpG island set identifies tissue-specificmethylation at developmental gene loci. PLoS Biol 2008, 6:e22.
21. Brinkman AB, Simmer F, Ma K, Kaan A, Zhu J, Stunnenberg HG: Whole-genome DNAmethylation profiling using MethyCap-seq. Methods 2010, 52:232-236.
22. Li Y, Zhu J, Tian G, Li N, Li Q, Ye M, Zheng H, Yu J, Wu H, Sun J, Zhang H, Chen Q, Luo R, Chen M, He Y, Jin X, Zhang Q, Yu C, Zhou G, Sun J, Huang Y, Zheng H, Cao H, Zhou X, Guo S, Hu X, Li X, Kristiansen K, Bolund L, Xu J, et al.: The DNA methylome of human peripheral blood mononuclear cells. PLoS Biol 2010, 8:e1.000533.
23. Bock C, Tomazou EM, Brinkman AB, Müller F, Simmer F, Gu H, Jäger N, Gnirke A, Stunnenberg HG, Meissner A: Quantitative comparison of genome-wide DNA methylationmapping technologies. Nat Biotechnol 2010, 28:1106-1114.
24. Harris RA, Wang T, Coarfa C, Nagarajan RP, Hong C, Downey SL, Johnson BE, Fouse SD, Delaney A, Zhao Y, Olshen A, Ballinger T, Zhou X, Forsberg KJ, Gu J, Echipare L, O'Geen H, Lister R, Pelizzola M, Xi Y, Epstein CB, Bernstein BE, Hawkins RD, Ren B, ChungWY, Gu H, Bock C, Gnirke A, Zhang MQ, Haussler D, et al.: Comparison of sequencing-basedmethods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nat Biotechnol 2010, 28:1097-1105.
25. Bell JT, Pai AA, Pickrell JK, Gaffney DJ, Pique-Regi R, Degner JF, Gilad Y, Pritchard JK: DNAmethylation patterns associate with genetic and gene expression variation in HapMap cell lines. Genome Biol 2011, 12:R10.
26. Pai AA, Bell JT, Marioni JC, Pritchard JK, Gilad Y: A genome-wide study of DNAmethylation patterns and gene expression levels in multiple human and chimpanzee tissues. PLoS Genet 2011, 7:e1001316.
27. Hellman A, Chess A: Gene body-specificmethylation on the active X chromosome. Science 2007, 315:1141-1143.
28. Ball MP, Li JB, Gao Y, Lee JH, LeProust EM, Park IH, Xie B, Daley GQ, Church GM: Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat Biotechnol 2009, 27:361-368.
29. Rauch TA, Wu X, Zhong X, Riggs AD, Pfeifer GP: A human B cell methylome at 100-base pair resolution. Proc Natl Acad Sci U S A 2009, 106:671-678.
30. Rountree MR, Selker EU: DNAmethylation inhibits elongation but not initiation of transcription in Neurospora crassa. Genes Dev 1997, 11:2383-2395.
31. Lorincz MC, Dickerson DR, Schmitt M, Groudine M: Intragenic DNA methylation alters chromatin structure and elongation efficiency in mammalian cells. Nat Struct Mol Biol 2004, 11:1068-1075.
32. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C, Fouse SD, Johnson BE, Hong C, Nielsen C, Zhao Y, Turecki G, Delaney A, Varhol R, Thiessen N, Shchors K, Heine VM, Rowitch DH, Xing X, Fiore C, Schillebeeckx M, Jones SJM, Haussler D, Marra MA, Hirst M, Wang T, Costello JF: Conserved role of intragenic DNAmethylation in regulating alternative promoters. Nature 2010, 466:253-257.
33. Choi JK, Bae J-B, Lyu J, Kim T-Y, Kim Y-J: Nucleosome deposition and DNAmethylation at coding region boundaries. Genome Biol 2009, 10:R89.
34. Cedar H, Bergman Y: Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 2009, 10:295-304.
35. Wu H, Coskun V, Tao J, Xie W, Ge W, Yoshikawa K, Li E, Zhang Y, Sun YE: Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 2010, 329:444-448.
36. Hahn MA, Wu X, Li AX, Hahn T, Pfeifer GP: Relationship between gene body DNAmethylation and intragenic H3K9me3 and H3K36me3 chromatinmarks. PLoS One 2011, 6:e18844.
37. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M, Hong J, James BP, Sarven S, Andrew PF: The human colon cancermethylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 2009, 41:178-186.
38. Akalin A, Garrett-Bakelman FE, Kormaksson M, Busuttil J, Zhang L, Khrebtukova I, Milne TA, Huang Y, Biswas D, Hess JL, Allis CD, Roeder RG, Valk PJM, Löwenberg B, Delwel R, Fernandez HF, Paietta E, Tallman MS, Schroth GP, Mason CE, Melnick A, Figueroa ME: Base-pair resolution DNAmethylation sequencing reveals profoundly divergent epigenetic landscapes in acute myeloid leukemia. PLoS Genet 2012, 8:e1002781.
39. Toperoff G, Aran D, Kark JD, Rosenberg M, Dubnikov T, Nissan B, Wainstein J, Friedlander Y, Levy-Lahad E, Glaser B, Hellman A: Genome-wide survey reveals predisposing diabetes type 2-related DNA methylation variations in human peripheral blood. HumMol Genet 2012, 21:371-383.
40. Ng CW, Yildirim F, Yap YS, Dalin S, Matthews BJ, Velez PJ, Labadorf A, Housman DE, Fraenkel E: Extensive changes in DNA methylation are associated with expression of mutant huntingtin. Proc Natl Acad Sci U S A 2013, 110:2354-2359.
41. Huang DW, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2008, 4:44-57.
42. McMullan CJ, Schernhammer ES, Rimm EB, Hu FB, Forman JP: Melatonin secretion and the incidence of type 2 diabetes. JAMA 2013, 309:1388-1396.
43. Breiman L: Random forests. Mach Learn 2001, 45:5-32.
44. Brenet F, Moh M, Funk P, Feierstein E, Viale AJ, Socci ND, Scandura JM: Dnamethylation of the first exon is tightly linked to transcriptional silencing. PLOS ONE 2011, 6:e14524.
45. Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, Meissner A, Kellis M, Marra MA, Beaudet AL, Ecker JR, Farnham PJ, Hirst M, Lander ES, Mikkelsen TS, Thomson JA: The NIH roadmap epigenomics mapping consortium. Nat Biotechnol, 28:1045-1048.
46. Cheng C, Yan K-K, Yip KY, Rozowsky J, Alexander R, Shou C, Gerstein M: A statistical framework formodeling gene expression using chromatin features with application tomodENCODE datasets. Genome Biol 2011, 12:R12.
47. Cheng C, Alexander R, Min R, Leng J, Yip KY, Rozowsky J, kiu Yan K, Dong X, Djebali S, Ruan Y, Davis CA, Carninci P, Lassman T, Gingeras TR, Serra RG, Birney E, Weng Z, Snyder M, Gerstein M: Understanding transcriptional regulation by integrative analysis of transcription factor binding data. Genome Res 2012, 22:1658-1667.
48. Zhou VW, Goren A, Bernstein BE: Charting histone modifications and the functional organization ofmammalian genomes. Nat Rev Genet 2011, 12:7-18.
49. Hohn T, Corsten S, Rieke S, Müller M, Rothnie H: Methylation of coding region alone inhibits gene expression in plant protoplasts. Proc Natl Acad Sci U S A 1996, 93:8334-8339.
50. Li X, Wang X, He K, Ma Y, Su N, He H, Stolc V, Tongprasit W, Jin W, Jiang J, Terzaghi W, Li S, Deng XW: High-resolutionmapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation histone methylation and gene expression. Plant Cell 2008, 25:259-276.
51. Flanagan JM, Wild L: An epigenetic role for noncoding RNAs and intragenic DNAmethylation. Genome Biol 2007, 8:307.
52. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE: Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNAmethylation patterning. Nature 2008, 452:215-219.
53. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, Xue C, Marinov GK, Khatun J, Williams BA, Zaleski C, Rozowsky J, Röder M, Kokocinski F, Abdelhamid RF, Alioto T, Antoshechkin I, Baer MT, Bar NS, Batut P, Bell K, Bell I, Chakrabortty S, Chen X, Chrast J, Curado J, et al.: Landscape of transcription in human cells. Nature 2012, 489:101-108.
54. Aran D, Sabato S, Hellman A: DNAmethylation of distal regulatory sites characterizes dysregulation of cancer genes. Genome Biol 2013, 14:R21.
55. Hayatsu H, Shiraishi M, Negishi K: Bisulfitemodification for analysis of DNAmethylation. Curr Protoc Nucleic Acid Chem 2008, 33:6.10.1-6.10.15.
56. Li R, Yu C, Li Y, Lam T-W, Yiu S-M, Kristiansen K, Wang J: SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 2009, 25:1966-1967.
57. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D: The human genome browser at UCSC. Genome Res 2002, 12:996-1006.
58. Li H, Durbin R: Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
59. Trapnell C, Pachter L, Salzberg SL: TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111.
60. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B: Mapping and quantifying mammalian transcriptomes by RNA-Seq. NatureMethods 2008, 5:621-628.
61. Robinson JT, Thorvaldsdottir H,WincklerW, Guttman M, Lander ES, Getz G, Mesirov JP: Integrative genomics viewer. Nat Biotechnol 2011, 29:24-26.
62. Krzywinski MI, Schein JE, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA: Circos: an information aesthetic for comparative genomics. Genome Res 2009, 19:1639-1645.
63. Benjamini Y, Hochberg Y: Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B 1995, 57:289-300.
64. Harrow J, Frankish A, Gonzalez JM, Tapanari E, Diekhans M, Kokocinski F, Aken BL, Barrell D, Zadissa A, Searle S, Barnes I, Bignell A, Boychenko V, Hunt T, Kay M, Mukherjee G, Rajan J, Despacio-Reyes G, Saunders G, Steward C, Harte R, Lin M, Howald C, Tanzer A, Derrien T, Chrast J, Walters N, Balasubramanian S, Pei B, Tress M, et al.: GENCODE: the reference human genome annotation for the ENCODE project. Genome Res 2012, 22:1760-1774.
65. Hall M, Frank E, Holmes G, Pfahringer B, Reutemann P, Witten IH: The WEKA datamining software: an update. SIGKDD Explorations 2009, 11:10-18.
66. Edgar R, Domrchev M, Lash AE: Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30:207-210.