Analyzing the cancer methylome through targeted bisulfite sequencing

Cancer Letters

Volumn 340, Issue 2, 2013, Pages 171-178

  Lee, Eun Joon ^a   Luo, Junfeng ^a   Wilson, James M ^a   Shi, Huidong ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

DNA methylation; Next generation sequencing; Targeted bisulfite sequencing

Indexed keywords

BISULFITE; CIRCULAR DNA; DNA FRAGMENT; GENOMIC DNA; SINGLE STRANDED DNA;

BIOINFORMATICS; DNA METHYLATION; DNA MODIFICATION; DNA SEQUENCE; DOWNSTREAM PROCESSING; EPIGENETICS; GENE EXPRESSION; GENE MAPPING; GENE SEQUENCE; GENETIC ASSOCIATION; HUMAN; NEXT GENERATION SEQUENCING; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SHORT SURVEY;

EID: 84887617516     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.10.040     Document Type: Review

References (72)

1. Bird A. The essentials of DNA methylation. Cell 1992, 70:5-8.
2. Craig J.M., Bickmore W.A. The distribution of CpG islands in mammalian chromosomes. Nat. Genet. 1994, 7:376-382.
3. Winnefeld M., Lyko F. The aging epigenome: DNA methylation from the cradle to the grave. Genome Biol. 2012, 13:165.
4. Bock C., Beerman I., Lien W.-H., Smith Z.D., Gu H., Boyle P., Gnirke A., Fuchs E., Rossi D.J., Meissner A. DNA Methylation dynamics during in vivo differentiation of blood and skin stem cells. Mol. Cell 2012, 47:633-647.
5. Anway M.D., Skinner M.K. Epigenetic transgenerational actions of endocrine disruptors. Endocrinol. 2006, 147:S43-49.
6. Jirtle R.L., Skinner M.K. Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 2007, 8:253-262.
7. Fraga M.F., Ballestar E., Paz M.F., Ropero S., Setien F., Ballestar M.L., Heine-Suner D., Cigudosa J.C., Urioste M., Benitez J., Boix-Chornet M., Sanchez-Aguilera A., Ling C., Carlsson E., Poulsen P., Vaag A., Stephan Z., Spector T.D., Wu Y.Z., Plass C., Esteller M. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl. Acad. Sci. USA 2005, 102:10604-10609.
8. Egger G., Liang G., Aparicio A., Jones P.A. Epigenetics in human disease and prospects for epigenetic therapy. Nature 2004, 429:457-463.
9. Irier H.A., Jin P. Dynamics of DNA methylation in aging and alzheimer's disease. DNA Cell Biol. 2012.
10. Jayaraman S. Epigenetics of autoimmune diabetes. Epigenomics 2011, 3:639-648.
11. Movassagh M., Vujic A., Foo R. Genome-wide DNA methylation in human heart failure. Epigenomics 2011, 3:103-109.
12. Robertson K.D. DNA methylation and human disease. Nat. Rev. Genet. 2005, 6:597-610.
13. Baylin S.B. DNA methylation and gene silencing in cancer. Nat. Clin. Pract. Oncol. 2005, 2(Suppl 1):S4-11.
14. Jones P.A., Baylin S.B. The epigenomics of cancer. Cell 2007, 128:683-692.
15. Jones P.A., Baylin S.B. The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 2002, 3:415-428.
16. Shi H., Wang M.X., Caldwell C.W. CpG islands: their potential as biomarkers for cancer. Expert Rev. Mol. Diagn. 2007, 7:519-531.
17. Yang X., Lay F., Han H., Jones P.A. Targeting DNA methylation for epigenetic therapy. Trends Pharmacol. Sci. 2010, 31:536-546.
18. Issa J.-P.J. DNA Methylation as a therapeutic target in cancer. Clin. Cancer Res. 2007, 13:1634-1637.
19. Callinan P.A., Feinberg A.P. The emerging science of epigenomics. Hum. Mol. Genet. 2006, 15:R95-R101.
20. Laird P.W. Principles and challenges of genome-wide DNA methylation analysis. Nat. Rev. Genet. 2010, 11:191-203.
21. Lister R., Ecker J.R. Finding the fifth base: genome-wide sequencing of cytosine methylation. Genome Res. 2009, 19:959-966.
22. Zilberman D., Henikoff S. Genome-wide analysis of DNA methylation patterns. Development 2007, 134:3959-3965.
23. Yan P.S., Chen C.M., Shi H., Rahmatpanah F., Wei S.H., Caldwell C.W., Huang T.H. Dissecting complex epigenetic alterations in breast cancer using CpG island microarrays. Cancer Res. 2001, 61:8375-8380.
24. Khulan B., Thompson R.F., Ye K., Fazzari M.J., Suzuki M., Stasiek E., Figueroa M.E., Glass J.L., Chen Q., Montagna C., Hatchwell E., Selzer R.R., Richmond T.A., Green R.D., Melnick A., Greally J.M. Comparative isoschizomer profiling of cytosine methylation: the HELP assay. Genome Res. 2006, 16:1046-1055.
25. Estecio M.R., Yan P.S., Ibrahim A.E., Tellez C.S., Shen L., Huang T.H., Issa J.P. High-throughput methylation profiling by MCA coupled to CpG island microarray. Genome Res. 2007, 17:1529-1536.
26. Weber M., Davies J.J., Wittig D., Oakeley E.J., Haase M., Lam W.L., Schubeler D. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat. Genet. 2005, 37:853-862.
27. Rauch T., Li H., Wu X., Pfeifer G.P. MIRA-Assisted microarray analysis, a new technology for the determination of DNA methylation patterns, identifies frequent methylation of homeodomain-containing genes in lung cancer cells. Cancer Res. 2006, 66:7939-7947.
28. Suzuki M., Jing Q., Lia D., Pascual M., McLellan A., Greally J. Optimized design and data analysis of tag-based cytosine methylation assays. Genome Biol. 2010, 11:R36.
29. Challen G.A., Sun D., Jeong M., Luo M., Jelinek J., Berg J.S., Bock C., Vasanthakumar A., Gu H., Xi Y., Liang S., Lu Y., Darlington G.J., Meissner A., Issa J.-P.J., Godley L.A., Li W., Goodell M.A. Dnmt3a is essential for hematopoietic stem cell differentiation. Nat. Genet. 2012, 44:23-31.
30. Harris R.A., Wang T., Coarfa C., Nagarajan R.P., Hong C., Downey S.L., Johnson B.E., Fouse S.D., Delaney A., Zhao Y., Olshen A., Ballinger T., Zhou X., Forsberg K.J., Gu J., Echipare L., O'Geen H., Lister R., Pelizzola M., Xi Y., Epstein C.B., Bernstein B.E., Hawkins R.D., Ren B., Chung W.Y., Gu H., Bock C., Gnirke A., Zhang M.Q., Haussler D., Ecker J.R., Li W., Farnham P.J., Waterland R.A., Meissner A., Marra M.A., Hirst M., Milosavljevic A., Costello J.F. Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nat. Biotechnol. 2010, 28:1097-1105.
31. Choi J.H., Li Y., Guo J., Pei L., Rauch T.A., Kramer R.S., Macmil S.L., Wiley G.B., Bennett L.B., Schnabel J.L., Taylor K.H., Kim S., Xu D., Sreekumar A., Pfeifer G.P., Roe B.A., Caldwell C.W., Bhalla K.N., Shi H. Genome-wide DNA methylation maps in follicular lymphoma cells determined by methylation-enriched bisulfite sequencing. PLoS One. 2010, 5:e13020.
32. Sandoval J., Heyn H., Moran S., Serra-Musach J., Pujana M.A., Bibikova M., Esteller M. Validation of a DNA methylation microarray for 450,000CpG sites in the human genome. Epigenetics 2011, 6:692-702.
33. Ehrich M., Nelson M.R., Stanssens P., Zabeau M., Liloglou T., Xinarianos G., Cantor C.R., Field J.K., van den Boom D. Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc. Natl. Acad. Sci. USA 2005, 102:15785-15790.
34. Laurent L., Wong E., Li G., Huynh T., Tsirigos A., Ong C.T., Low H.M., Kin Sung K.W., Rigoutsos I., Loring J., Wei C.L. Dynamic changes in the human methylome during differentiation. Genome Res. 2010, 20:320-331.
35. Lister R., Pelizzola M., Dowen R.H., Hawkins R.D., Hon G., Tonti-Filippini J., Nery J.R., Lee L., Ye Z., Ngo Q.M., Edsall L., Antosiewicz-Bourget J., Stewart R., Ruotti V., Millar A.H., Thomson J.A., Ren B., Ecker J.R. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009, 462:315-322.
36. 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., Huang Y., Cao H., Zhou X., Guo S., Hu X., Li X., Kristiansen K., Bolund L., Xu J., Wang W., Yang H., Wang J., Li R., Beck S., Zhang X. The DNA methylome of human peripheral blood mononuclear cells. PLoS Biol. 2010, 8:e1000533.
37. Hodges E., Molaro A., Dos Santos C.O., Thekkat P., Song Q., Uren P.J., Park J., Butler J., Rafii S., McCombie W.R., Smith A.D., Hannon G.J. Directional DNA methylation changes and complex intermediate states accompany lineage specificity in the adult hematopoietic compartment. Mol. Cell 2011, 44:17-28.
38. Berman B.P., Weisenberger D.J., Aman J.F., Hinoue T., Ramjan Z., Liu Y., Noushmehr H., Lange C.P., van Dijk C.M., Tollenaar R.A., Van Den Berg D., Laird P.W. Regions of focal DNA hypermethylation and long-range hypomethylation in colorectal cancer coincide with nuclear lamina-associated domains. Nat. Genet. 2012, 44:40-46.
39. Hon G.C., Hawkins R.D., Caballero O.L., Lo C., Lister R., Pelizzola M., Valsesia A., Ye Z., Kuan S., Edsall L.E., Camargo A.A., Stevenson B.J., Ecker J.R., Bafna V., Strausberg R.L., Simpson A.J., Ren B. Global DNA hypomethylation coupled to repressive chromatin domain formation and gene silencing in breast cancer. Genome Res. 2012, 22:246-258.
40. Hansen K.D., Timp W., Bravo H.C., Sabunciyan S., Langmead B., McDonald O.G., Wen B., Wu H., Liu Y., Diep D., Briem E., Zhang K., Irizarry R.A., Feinberg A.P. Increased methylation variation in epigenetic domains across cancer types. Nat. Genet. 2011, 43:768-775.
41. Porreca G.J., Zhang K., Li J.B., Xie B., Austin D., Vassallo S.L., LeProust E.M., Peck B.J., Emig C.J., Dahl F., Gao Y., Church G.M., Shendure J. Multiplex amplification of large sets of human exons. Nat. Methods 2007, 4:931-936.
42. Okou D.T., Steinberg K.M., Middle C., Cutler D.J., Albert T.J., Zwick M.E. Microarray-based genomic selection for high-throughput resequencing. Nat. Methods 2007, 4:907-909.
43. Albert T.J., Molla M.N., Muzny D.M., Nazareth L., Wheeler D., Song X., Richmond T.A., Middle C.M., Rodesch M.J., Packard C.J., Weinstock G.M., Gibbs R.A. Direct selection of human genomic loci by microarray hybridization. Nat. Methods 2007, 4:903-905.
44. Hodges E., Xuan Z., Balija V., Kramer M., Molla M.N., Smith S.W., Middle C.M., Rodesch M.J., Albert T.J., Hannon G.J., McCombie W.R. Genome-wide in situ exon capture for selective resequencing. Nat. Genet. 2007, 39:1522-1527.
45. Porreca G.J., Zhang K., Li J.B., Xie B., Austin D., Vassallo S.L., LeProust E.M., Peck B.J., Emig C.J., Dahl F., Gao Y., Church G.M., Shendure J. Multiplex amplification of large sets of human exons. Nat. Methods 2007, 4:931-936.
46. Deng J., Shoemaker R., Xie B., Gore A., LeProust E.M., Antosiewicz-Bourget J., Egli D., Maherali N., Park I.H., Yu J., Daley G.Q., Eggan K., Hochedlinger K., Thomson J., Wang W., Gao Y., Zhang K. Targeted bisulfite sequencing reveals changes in DNA methylation associated with nuclear reprogramming. Nat. Biotechnol. 2009, 27:353-360.
47. Ball M.P., Li J.B., Gao Y., Lee J.-H., LeProust E.M., Park I.-H., Xie B., Daley G.Q., Church G.M. Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat. Biotechnol. 2009, 27:361-368.
48. Diep D., Plongthongkum N., Gore A., Fung H.L., Shoemaker R., Zhang K. Library-free methylation sequencing with bisulfite padlock probes. Nat. Methods 2012, 9:270-272.
49. Gnirke A., Melnikov A., Maguire J., Rogov P., LeProust E.M., Brockman W., Fennell T., Giannoukos G., Fisher S., Russ C., Gabriel S., Jaffe D.B., Lander E.S., Nusbaum C. Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing. Nat. Biotechnol. 2009, 27:182-189.
50. Lee E.J., Pei L., Srivastava G., Joshi T., Kushwaha G., Choi J.H., Robertson K.D., Wang X., Colbourne J.K., Zhang L., Schroth G.P., Xu D., Zhang K., Shi H. Targeted bisulfite sequencing by solution hybrid selection and massively parallel sequencing. Nucl. Acids Res. 2011, 39:e127.
51. Wang J., Jiang H., Ji G., Gao F., Wu M., Sun J., Luo H., Wu J., Wu R., Zhang X. High resolution profiling of human exon methylation by liquid hybridization capture-based bisulfite sequencing. BMC Genomics 2011, 12:597.
52. Harrow J., Denoeud F., Frankish A., Reymond A., Chen C.-K., Chrast J., Lagarde J., Gilbert J., Storey R., Swarbreck D., Rossier C., Ucla C., Hubbard T., Antonarakis S., Guigo R. GENCODE: producing a reference annotation for ENCODE. Genome Biol. 2006, 7:S4.
53. Nautiyal S., Carlton V.E., Lu Y., Ireland J.S., Flaucher D., Moorhead M., Gray J.W., Spellman P., Mindrinos M., Berg P., Faham M. High-throughput method for analyzing methylation of CpGs in targeted genomic regions. Proc. Natl. Acad. Sci. USA 2010, 107:12587-12592.
54. Albert T.J., Molla M.N., Muzny D.M., Nazareth L., Wheeler D., Song X., Richmond T.A., Middle C.M., Rodesch M.J., Packard C.J., Weinstock G.M., Gibbs R.A. Direct selection of human genomic loci by microarray hybridization. Nat. Methods 2007, 4:903-905.
55. Okou D.T., Steinberg K.M., Middle C., Cutler D.J., Albert T.J., Zwick M.E. Microarray-based genomic selection for high-throughput resequencing. Nat. Methods 2007, 4:907-909.
56. Hodges E., Smith A.D., Kendall J., Xuan Z., Ravi K., Rooks M., Zhang M.Q., Ye K., Bhattacharjee A., Brizuela L., McCombie W.R., Wigler M., Hannon G.J., Hicks J.B. High definition profiling of mammalian DNA methylation by array capture and single molecule bisulfite sequencing. Genome Res. 2009, 19:1593-1605.
57. Taylor K.H., Kramer R.S., Davis J.W., Guo J., Duff D.J., Xu D., Caldwell C.W., Shi H. Ultradeep bisulfite sequencing analysis of DNA methylation patterns in multiple gene promoters by 454 sequencing. Cancer Res. 2007, 67:8511-8518.
58. Varley K.E., Mitra R.D. Bisulfite Patch PCR enables multiplexed sequencing of promoter methylation across cancer samples. Genome Res. 2010, 20:1279-1287.
59. Tewhey R., Warner J.B., Nakano M., Libby B., Medkova M., David P.H., Kotsopoulos S.K., Samuels M.L., Hutchison J.B., Larson J.W., Topol E.J., Weiner M.P., Harismendy O., Olson J., Link D.R., Frazer K.A. Microdroplet-based PCR enrichment for large-scale targeted sequencing. Nat. Biotechnol. 2009, 27:1025-1031.
60. Komori H.K., LaMere S.A., Torkamani A., Hart G.T., Kotsopoulos S., Warner J., Samuels M.L., Olson J., Head S.R., Ordoukhanian P., Lee P.L., Link D.R., Salomon D.R. Application of microdroplet PCR for large-scale targeted bisulfite sequencing. Genome Res. 2011, 21:1738-1745.
61. Srivastava G.P., Guo J., Shi H., Xu D. PRIMEGENS-v2: genome-wide primer design for analyzing DNA methylation patterns of CpG islands. Bioinformatics 2008, 24:1837-1842.
62. Krueger F., Kreck B., Franke A., Andrews S.R. DNA methylome analysis using short bisulfite sequencing data. Nat. Methods 2012, 9:145-151.
63. Xi Y., Li W. BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinformatics 2009, 10:232.
64. Chen P.Y., Cokus S.J., Pellegrini M. BS Seeker: precise mapping for bisulfite sequencing. BMC Bioinformatics 2010, 11:203.
65. Krueger F., Andrews S.R. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 2011, 27:1571-1572.
66. Harris E.Y., Ponts N., Levchuk A., Roch K.L., Lonardi S. BRAT: bisulfite-treated reads analysis tool. Bioinformatics 2010, 26:572-573.
67. Smith A.D., Chung W.Y., Hodges E., Kendall J., Hannon G., Hicks J., Xuan Z., Zhang M.Q. Updates to the RMAP short-read mapping software. Bioinformatics 2009, 25:2841-2842.
68. Pedersen B., Hsieh T.F., Ibarra C., Fischer R.L. MethylCoder: software pipeline for bisulfite-treated sequences. Bioinformatics 2011, 27:2435-2436.
69. Kreck B., Marnellos G., Richter J., Krueger F., Siebert R., Franke A. B-SOLANA: an approach for the analysis of two-base encoding bisulfite sequencing data. Bioinformatics 2012, 28:428-429.
70. Li R., Li Y., Kristiansen K., Wang J. SOAP: short oligonucleotide alignment program. Bioinformatics 2008, 24:713-714.
71. Langmead B., Trapnell C., Pop M., Salzberg S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009, 10:R25.
72. Flusberg B.A., Webster D.R., Lee J.H., Travers K.J., Olivares E.C., Clark T.A., Korlach J., Turner S.W. Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat. Methods 2010, 7:461-465.