Direct ChIP-bisulfite sequencing reveals a role of H3K27me3 mediating aberrant hypermethylation of promoter CpG islands in cancer cells

Genomics

Volumn 103, Issue 2-3, 2014, Pages 204-210

  Gao, Fei ^a   Ji, Guanyu ^a   Gao, Zhaowei ^a   Han, Xu ^a   Ye, Mingzhi ^a   Yuan, Zhimei ^a   Luo, Huijuan ^a   Huang, Xiaojun ^a,e   Natarajan, Karthikraj ^a   Wang, Jun ^a,b,c,d   Yang, Huanming ^a   Zhang, Xiuqing ^a  

^a BGI SHENZHEN   (China)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^d Capital Region   (Denmark)

^e WUHAN UNIVERSITY   (China)

Author keywords

Chromatin immunoprecipitation; CpG Island; DNA methylation; Gastric cancer

Indexed keywords

BISULFITE; HISTONE; HISTONE H3K27ME3; UNCLASSIFIED DRUG; DNA; TUMOR PROTEIN;

ARTICLE; CANCER CELL; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DEMETHYLATION; DNA METHYLATION; GENE ONTOLOGY; GENETIC ASSOCIATION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; MALE; PRIORITY JOURNAL; PROTEIN MICROARRAY; TUMOR GENE; DNA SEQUENCE; GENETICS; METABOLISM; NEOPLASM; PROMOTER REGION; TUMOR CELL LINE;

CELL LINE, TUMOR; CPG ISLANDS; DNA METHYLATION; DNA, NEOPLASM; HISTONES; HUMANS; NEOPLASM PROTEINS; NEOPLASMS; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, DNA;

EID: 84898032380     PISSN: 08887543     EISSN: 10898646     Source Type: Journal    
DOI: 10.1016/j.ygeno.2013.12.006     Document Type: Article

References (42)

1. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
2. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002, 16:6-21.
3. Goll M.G., Bestor T.H. Eukaryotic cytosine methyltransferases. Ann. Rev. Biochem. 2005, 74:481-514.
4. Margueron R., Trojer P., Reinberg D. The key to development: interpreting the histone code?. Curr. Opin. Genet. Dev. 2005, 15:163-176.
5. Berdasco M., Esteller M. Aberrant epigenetic landscape in cancer: how cellular identity goes awry. Dev. Cell 2010, 19:698-711.
6. Jones P.A., Baylin S.B. The epigenomics of cancer. Cell 2007, 128:683-692.
7. Bestor T.H. Unanswered questions about the role of promoter methylation in carcinogenesis. Ann. N. Y. Acad. Sci. 2003, 983:22-27.
8. Deaton A.M., Bird A. CpG islands and the regulation of transcription. Genes Dev. 2011, 25:1010-1022.
9. Sproul D., Nestor C., Culley J., Dickson J.H., Dixon J.M., Harrison D.J., Meehan R.R., Sims A.H., Ramsahoye B.H. Transcriptionally repressed genes become aberrantly methylated and distinguish tumors of different lineages in breast cancer. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:4364-4369.
10. Sproul D., Kitchen R.R., Nestor C.E., Dixon J.M., Sims A.H., Harrison D.J., Ramsahoye B.H., Meehan R.R. Tissue of origin determines cancer-associated CpG island promoter hypermethylation patterns. Genome Biol. 2012, 13:R84.
11. Ohm J.E., McGarvey K.M., Yu X., Cheng L., Schuebel K.E., Cope L., Mohammad H.P., Chen W., Daniel V.C., Yu W., et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat. Genet. 2007, 39:237-242.
12. Easwaran H., Johnstone S.E., Van Neste L., Ohm J., Mosbruger T., Wang Q., Aryee M.J., Joyce P., Ahuja N., Weisenberger D., et al. A DNA hypermethylation module for the stem/progenitor cell signature of cancer. Genome Res. 2012, 22:837-849.
13. Bernstein B.E., Mikkelsen T.S., Xie X., Kamal M., Huebert D.J., Cuff J., Fry B., Meissner A., Wernig M., Plath K., et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006, 125:315-326.
14. Vire E., Brenner C., Deplus R., Blanchon L., Fraga M., Didelot C., Morey L., Van Eynde A., Bernard D., Vanderwinden J.M., et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006, 439:871-874.
15. Gal-Yam E.N., Egger G., Iniguez L., Holster H., Einarsson S., Zhang X., Lin J.C., Liang G., Jones P.A., Tanay A. Frequent switching of Polycomb repressive marks and DNA hypermethylation in the PC3 prostate cancer cell line. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:12979-12984.
16. Brinkman A.B., Gu H., Bartels S.J., Zhang Y., Matarese F., Simmer F., Marks H., Bock C., Gnirke A., Meissner A., Stunnenberg H.G. Sequential ChIP-bisulfite sequencing enables direct genome-scale investigation of chromatin and DNA methylation cross-talk. Genome Res. 2012, 22:1128-1138.
17. Statham A.L., Robinson M.D., Song J.Z., Coolen M.W., Stirzaker C., Clark S.J. Bisulphite-sequencing of chromatin immunoprecipitated DNA (BisChIP-seq) directly informs methylation status of histone-modified DNA. Genome Res. 2012, 22:1120-1127.
18. Li G., Ma L., Song C., Yang Z., Wang X., Huang H., Li Y., Li R., Zhang X., Yang H., Wang J. The YH database: the first Asian diploid genome database. Nucleic Acids Res. 2009, 37:D1025-D1028.
19. 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.
20. Song Q., Smith A.D. Identifying dispersed epigenomic domains from ChIP-Seq data. Bioinformatics 2011, 27:870-871.
21. 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. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009, 462:315-322.
22. Mortazavi A., Williams B.A., McCue K., Schaeffer L., Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 2008, 5:621-628.
23. Cuddapah S., Jothi R., Schones D.E., Roh T.Y., Cui K., Zhao K. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res. 2009, 19:24-32.
24. Weber M., Hellmann I., Stadler M.B., Ramos L., Paabo S., Rebhan M., Schubeler D. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat. Genet. 2007, 39:457-466.
25. Fuks F. DNA methylation and histone modifications: teaming up to silence genes. Curr. Opin. Genet. Dev. 2005, 15:490-495.
26. Severson P.L., Tokar E.J., Vrba L., Waalkes M.P., Futscher B.W. Coordinate H3K9 and DNA methylation silencing of ZNFs in toxicant-induced malignant transformation. Epigenetics 2013, 8.
27. Moison C., Senamaud-Beaufort C., Fourriere L., Champion C., Ceccaldi A., Lacomme S., Daunay A., Tost J., Arimondo P.B., Guieysse-Peugeot A.L. DNA methylation associated with polycomb repression in retinoic acid receptor beta silencing. FASEB J. 2013, 27:1468-1478.
28. Gonzalez M., Li F. DNA replication, RNAi and epigenetic inheritance. Epigenetics 2012, 7:14-19.
29. Simon S.A., Meyers B.C. Small RNA-mediated epigenetic modifications in plants. Curr. Opin. Plant Biol. 2011, 14:148-155.
30. Jia D., Jurkowska R.Z., Zhang X., Jeltsch A., Cheng X. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 2007, 449:248-251.
31. Ooi S.K., Qiu C., Bernstein E., Li K., Jia D., Yang Z., Erdjument-Bromage H., Tempst P., Lin S.P., Allis C.D., et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 2007, 448:714-717.
32. Mikkelsen T.S., Ku M., Jaffe D.B., Issac B., Lieberman E., Giannoukos G., Alvarez P., Brockman W., Kim T.K., Koche R.P., et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560.
33. Pan G., Tian S., Nie J., Yang C., Ruotti V., Wei H., Jonsdottir G.A., Stewart R., Thomson J.A. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 2007, 1:299-312.
34. Zhao X.D., Han X., Chew J.L., Liu J., Chiu K.P., Choo A., Orlov Y.L., Sung W.K., Shahab A., Kuznetsov V.A., et al. Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 2007, 1:286-298.
35. Ke X.S., Qu Y., Rostad K., Li W.C., Lin B., Halvorsen O.J., Haukaas S.A., Jonassen I., Petersen K., Goldfinger N., et al. Genome-wide profiling of histone h3 lysine 4 and lysine 27 trimethylation reveals an epigenetic signature in prostate carcinogenesis. PloS One 2009, 4:e4687.
36. Buck-Koehntop B.A., Defossez P.A. On how mammalian transcription factors recognize methylated DNA. Epigenetics 2013, 8:131-137.
37. Pedersen S.F., Stock C. Ion channels and transporters in cancer: Pathophysiology, regulation and clinical potential. Cancer Res. 2013, 73:1658-1661.
38. Prevarskaya N., Skryma R., Shuba Y. Targeting Ca(2+) transport in cancer: close reality or long perspective?. Expert Opin. Ther. Targets 2013, 17:225-241.
39. Faryna M., Konermann C., Aulmann S., Bermejo J.L., Brugger M., Diederichs S., Rom J., Weichenhan D., Claus R., Rehli M., et al. Genome-wide methylation screen in low-grade breast cancer identifies novel epigenetically altered genes as potential biomarkers for tumor diagnosis. FASEB J. 2012, 26:4937-4950.
40. Bauerschlag D.O., Ammerpohl O., Brautigam K., Schem C., Lin Q., Weigel M.T., Hilpert F., Arnold N., Maass N., Meinhold-Heerlein I., Wagner W. Progression-free survival in ovarian cancer is reflected in epigenetic DNA methylation profiles. Oncology 2011, 80:12-20.
41. Wang S.S., Smiraglia D.J., Wu Y.Z., Ghosh S., Rader J.S., Cho K.R., Bonfiglio T.A., Nayar R., Plass C., Sherman M.E. Identification of novel methylation markers in cervical cancer using restriction landmark genomic scanning. Cancer Res. 2008, 68:2489-2497.
42. Brune K., Hong S.M., Li A., Yachida S., Abe T., Griffith M., Yang D., Omura N., Eshleman J., Canto M., et al. Genetic and epigenetic alterations of familial pancreatic cancers. Cancer Epidemiol. Biomarkers Prev. 2008, 17:3536-3542.