Modeling complex patterns of differential DNA methylation that associate with gene expression changes

Nucleic Acids Research

Volumn 45, Issue 9, 2017, Pages 5100-5111

  Schlosberg, Christopher E ^a   VanderKraats, Nathan D ^a   Edwards, John R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BISULFITE; DNA; MESSENGER RNA;

ARTICLE; CANCER GENETICS; CELL LINEAGE; CELLS BY BODY ANATOMY; CLASSIFIER; COLON CANCER CELL LINE; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERMETHOD COMPARISON; PREDICTION; PRIORITY JOURNAL; PROMOTER REGION; RANDOM FOREST; RNA SEQUENCE; SEQUENCE ANALYSIS; SEQUENCE DATABASE; SUPERVISED MACHINE LEARNING; BIOLOGICAL MODEL; COLON TUMOR; DNA SEQUENCE; EVALUATION STUDY; GENE EXPRESSION REGULATION; GENETICS; HEMATOPOIESIS; HUMAN GENOME; NUCLEOTIDE SEQUENCE;

BASE SEQUENCE; COLONIC NEOPLASMS; DNA METHYLATION; EPIGENOMICS; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME, HUMAN; HEMATOPOIESIS; HUMANS; MODELS, GENETIC; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, RNA;

EID: 85027177188     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkx078     Document Type: Article

References (51)

1. Smith,Z.D. and Meissner,A. (2013) DNA methylation: roles in mammalian development. Nat. Rev. Genet., 14, 204-220.
2. Laurent,L., Wong,E., Li,G., Huynh,T., Tsirigos,A., Ong,C.T., Low,H.M., Kin Sung,K.W., Rigoutsos,I., Loring,J. et al. (2010) Dynamic changes in the human methylome during differentiation. Genome Res., 20, 320-331.
3. Laird,P.W. and Jaenisch,R. (1994) DNA methylation and cancer. Hum. Mol. Genet., 3(suppl. 1), 1487-1495.
4. Baylin,S.B., Esteller,M., Rountree,M.R., Bachman,K.E., Schuebel,K. and Herman,J.G. (2001) Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum. Mol. Genet., 10, 687-692.
5. 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. et al. (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature, 462, 315-322.
6. Ehrlich,M. (2002) DNA methylation in cancer: too much, but also too little. Oncogene, 21, 5400-5413.
7. Keshet,I., Schlesinger,Y., Farkash,S., Rand,E., Hecht,M., Segal,E., Pikarski,E., Young,R.A., Niveleau,A., Cedar,H. et al. (2006) Evidence for an instructive mechanism of de novo methylation in cancer cells. Nat. Genet., 38, 149-153.
8. Bird,A. (2002) DNA methylation patterns and epigenetic memory. Genes Dev., 16, 6-21.
9. Suzuki,M.M. and Bird,A. (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet., 9, 465-476.
10. Bock,C. (2012) Analysing and interpreting DNA methylation data. Nat. Rev. Genet., 13, 705-719.
11. Wagner,J.R., Busche,S., Ge,B., Kwan,T., Pastinen,T. and Blanchette,M. (2014) The relationship between DNA methylation, genetic and expression inter-individual variation in untransformed human fibroblasts. Genome Biol., 15, R37.
12. Schultz,M.D., He,Y., Whitaker,J.W., Hariharan,M.,Mukamel,E.A., Leung,D., Rajagopal,N., Nery,J.R., Urich,M.A., Chen,H. et al. (2015) Human body epigenome maps reveal noncanonical DNA methylation variation. Nature, 523, 212-216.
13. Kulis,M., Heath,S., Bibikova,M., Queiros,A.C., Navarro,A., Clot,G., Martinez-Trillos,A., Castellano,G., Brun-Heath,I., Pinyol,M. et al. (2012) Epigenomic analysis detects widespread gene-body DNA hypomethylation in chronic lymphocytic leukemia. Nat. Genet., 44, 1236-1242.
14. Proudhon,C., Duffié,R., Ajjan,S., Cowley,M., Iranzo,J., Carbajosa,G., Saadeh,H., Holland,M.L., Oakey,R.J., Rakyan,V.K. et al. (2012) Protection against de novo methylation is instrumental in maintaining parent-of-origin methylation inherited from the gametes. Mol. Cell, 47, 909-920.
15. van Eijk,K.R., de Jong,S., Boks,M.P., Langeveld,T., Colas,F., Veldink,J.H., de Kovel,C.G., Janson,E., Strengman,E., Langfelder,P. et al. (2012) Genetic analysis of DNA methylation and gene expression levels in whole blood of healthy human subjects. BMC Genomics, 13, 1-13.
16. Vanderkraats,N.D., Hiken,J.F., Decker,K.F. and Edwards,J.R. (2013) Discovering high-resolution patterns of differential DNA methylation that correlate with gene expression changes. Nucleic Acids Res., 41, 6816-6827.
17. Irizarry,R.A., Ladd-Acosta,C.,Wen,B., Wu,Z., Montano,C., Onyango,P., Cui,H., Gabo,K., Rongione,M., Webster,M. et al. (2009) The human colon cancer methylome shows similar hypo-and hypermethylation at conserved tissue-specific CpG island shores. Nat. Genet., 41, 178-186.
18. Yang,X., Han,H., De Carvalho,D.D., Lay,F.D., Jones,P.A. and Liang,G. (2014) Gene body methylation can alter gene expression and is a therapeutic target in cancer. Cancer Cell, 26, 577-590.
19. Ball,M.P., Li,J.B., Gao,Y., Lee,J.-H., LeProust,E.M., Park,I.-H., Xie,B., Daley,G.Q. and Church,G.M. (2009) Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat. Biotech., 27, 361-368.
20. Cruickshanks,H.A., McBryan,T., Nelson,D.M., VanderKraats,N.D., Shah,P.P., van Tuyn,J., Rai,T.S., Brock,C., Donahue,G., Dunican,D.S. et al. (2013) Senescent cells harbour features of the cancer epigenome. Nat. Cell Biol., 15, 1495-1506.
21. Lund,K., Cole,J.J., VanderKraats,N.D., McBryan,T., Pchelintsev,N.A., Clark,W., Copland,M., Edwards,J.R. and Adams,P.D. (2014) DNMT inhibitors reverse a specific signature of aberrant promoter DNA methylation and associated gene silencing in AML. Genome Biol., 15, 1906-1920.
22. Consortium,R.E., Kundaje,A., Meuleman,W., Ernst,J., Bilenky,M., Yen,A., Heravi-Moussavi,A., Kheradpour,P., Zhang,Z.,Wang,J. et al. (2015) Integrative analysis of 111 reference human epigenomes. Nature, 518, 317-330.
23. Wu,C., MacLeod,I. and Su,A.I. (2013) BioGPS and MyGene.info: organizing online, gene-centric information. Nucleic Acids Res., 41, D561-D565.
24. Kent,W.J., Sugnet,C.W., Furey,T.S., Roskin,K.M., Pringle,T.H., Zahler,A.M. and Haussler,A.D. (2002) The human genome browser at UCSC. Genome Res., 12, 996-1006.
25. Adams,D., Altucci,L., Antonarakis,S.E., Ballesteros,J., Beck,S., Bird,A., Bock,C., Boehm,B., Campo,E., Caricasole,A. et al. (2012) BLUEPRINT to decode the epigenetic signature written in blood. Nat. Biotech., 30, 224-226.
26. Blattler,A., Yao,L., Witt,H., Guo,Y., Nicolet,C.M., Berman,B.P. and Farnham,P.J. (2014) Global loss of DNA methylation uncovers intronic enhancers in genes showing expression changes. Genome Biol., 15, 327-316.
27. Jjingo,D., Conley,A.B., Yi,S.V., Lunyak,V.V. and Jordan,I.K. (2012) On the presence and role of human gene-body DNA methylation. Oncotarget, 3, 462-474.
28. Wu,H., Xu,T., Feng,H., Chen,L., Li,B., Yao,B., Qin,Z., Jin,P. and Conneely,K.N. (2015) Detection of differentially methylated regions from whole-genome bisulfite sequencing data without replicates. Nucleic Acids Res., 43, e141.
29. Lou,S., Lee,H.-M., Qin,H., Li,J.-W., Gao,Z., Liu,X., Chan,L.L., Lam,V.K.L., So,W.-Y., Wang,Y. et al. (2014) Whole-genome bisulfite sequencing of multiple individuals reveals complementary roles of promoter and gene body methylation in transcriptional regulation. Genome Biol., 15, 6-21.
30. Eckhardt,F., Lewin,J., Cortese,R., Rakyan,V.K., Attwood,J., Burger,M., Burton,J., Cox,T.V., Davies,R., Down,T.A. et al. (2006) DNA methylation profiling of human chromosomes 6, 20 and Nat. Genet., 38, 1378-1385.
31. Hansen,K.D., Langmead,B. and Irizarry,R.A. (2012) BSmooth: from whole genome bisulfite sequencing reads to differentially methylated regions. Genome Biol., 13, R83.
32. Breiman,L. (2001) Random Forests. Mach. Learn., 45, 5-32.
33. Pedregosa,F., Varoquaux,G., Gramfort,A.,Michel,V., Thirion,B., Grisel,O., Blondel,M., Prettenhofer,P., Weiss,R., Dubourg,V. et al. (2011) Scikit-learn: machine learning in python. J. Mach. Learn. Res., 12, 2825-2830.
34. Albanese,D., Visintainer,R., Merler,S., Riccadonna,S., Jurman,G. and Furlanello,C. (2012) mlpy: machine learning python. arXiv, 1-4.
35. Kretzmer,H., Bernhart,S.H.,Wang,W., Haake,A., Weniger,M.A., Bergmann,A.K., Betts,M.J., Carrillo-de-Santa-Pau,E., Doose,G., Gutwein,J. et al. (2015) DNA methylome analysis in Burkitt and follicular lymphomas identifies differentially methylated regions linked to somatic mutation and transcriptional control. Nat. Genet., 47, 1316-1325.
36. Sakoe,H. and Chiba,S. (1978) Dynamic Programming Algorithm Optimization for Spoken Word Recognition. IEEE Trans. Acoust. Speech, Signal Process., 26, 43-49.
37. Huang,D.W., Sherman,B.T. and Lempicki,R.A. (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
38. Hsieh,C.L. (1994) Dependence of transcriptional repression on CpG methylation density. Mol. Cell. Biol., 14, 5487-5494.
39. Deaton,A.M. and Bird,A. (2011) CpG islands and the regulation of transcription. Genes Dev., 25, 1010-1022.
40. Varley,K.E., Gertz,J., Bowling,K.M., Parker,S.L., Reddy,T.E., Pauli-Behn,F., Cross,M.K., Williams,B.A., Stamatoyannopoulos,J.A., Crawford,G.E. et al. (2013) Dynamic DNA methylation across diverse human cell lines and tissues. Genome Res., 23, 555-567.
41. Jones,P.A. (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet., 13, 484-492.
42. Bocker,M.T., Hellwig,I., Breiling,A., Eckstein,V., Ho,A.D. and Lyko,F. (2011) Genome-wide promoter DNA methylation dynamics of human hematopoietic progenitor cells during differentiation and aging. Blood, 117, e182-e189.
43. Kulis,M., Merkel,A., Heath,S., Queiros,A.C., Schuyler,R.P., Castellano,G., Beekman,R., Raineri,E., Esteve,A., Clot,G. et al. (2015) Whole-genome fingerprint of the DNA methylome during human B cell differentiation. Nat. Genet., 47, 746-756.
44. Severson,P.L., Tokar,E.J., Vrba,L., Waalkes,M.P. and Futscher,B.W. (2014) Coordinate H3K9 and DNA methylation silencing of ZNFs in toxicant-induced malignant transformation. Epigenetics, 8, 1080-1088.
45. Herman,J.G. and Baylin,S.B. (2003) Gene silencing in cancer in association with promoter hypermethylation. N. Engl. J. Med., 349, 2042-2054.
46. Robertson,K.D. (2005) DNA methylation and human disease. Nat. Rev. Genet., 6, 597-610.
47. Bestor,T.H., Edwards,J.R. and Boulard,M. (2015) Notes on the role of dynamic DNA methylation in mammalian development. Proc. Natl. Acad. Sci. U.S.A., 112, 6796-6799.
48. Moarii,M., Boeva,V., Vert,J.-P. and Reyal,F. (2015) Changes in correlation between promoter methylation and gene expression in cancer. BMC Genomics, 16, 873.
49. Hovestadt,V., Jones,D.T.W., Picelli,S., Wang,W., Kool,M., Northcott,P.A., Sultan,M., Stachurski,K., Ryzhova,M., Warnatz,H.-J. et al. (2014) Decoding the regulatory landscape of medulloblastoma using DNA methylation sequencing. Nature, 510, 537-541.
50. Hodges,E., Molaro,A., Dos Santos,C.O., Thekkat,P., Song,Q., Uren,P.J., Park,J., Butler,J., Rafii,S., McCombie,W.R. et al. Directional DNA methylation changes and complex intermediate states accompany lineage specificity in the adult hematopoietic compartment. Mol. Cell, 44, 17-28.
51. Azad,N., Zahnow,C.A., Rudin,C.M. and Baylin,S.B. (2013) The future of epigenetic therapy in solid tumours-lessons from the past. Nat. Rev. Clin. Oncol., 10, 256-266.