Hypomethylation coordinates antagonistically with hypermethylation in cancer development: A case study of leukemia

Human Genomics

Volumn 10, Issue , 2016, Pages

  Kushwaha, Garima ^a   Dozmorov, Mikhail ^b   Wren, Jonathan D ^c   Qiu, Jing ^d   Shi, Huidong ^e   Xu, Dong ^a,f  

^a UNIVERSITY OF MISSOURI   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^d UNIVERSITY OF DELAWARE   (United States)

^e MEDICAL COLLEGE OF GEORGIA   (United States)

^f University of Missouri   (United States)

Author keywords

3 UTR; Cancer; CLL; DNA methylation; Enhancer; Epigenetic regulation; Hypomethylation; Signaling pathway

Indexed keywords

B LYMPHOCYTE RECEPTOR; POLYCOMB REPRESSIVE COMPLEX 2; PROTEIN; PROTEIN P53; SUZ12 PROTEIN; TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR EZH2; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; HISTONE; TUMOR MARKER;

3' UNTRANSLATED REGION; APOPTOSIS; ARTICLE; B CELL CHRONIC LYMPHOCYTE LEUKEMIA; B CELL LEUKEMIA; BINDING SITE; CALCIUM SIGNALING; CASE STUDY; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMATIN; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL ARTICLE; CONTROLLED STUDY; DNA METHYLATION; ENHANCER REGION; EXON; GENE EXPRESSION; GENE ONTOLOGY; GENETIC BACKGROUND; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; INTRON; LEUKOCYTE ACTIVATION; OVERLAPPING GENE; PHENOTYPE; PROMOTER REGION; BIOLOGICAL MODEL; CPG ISLAND; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETIC HETEROGENEITY; GENETICS; GENOME-WIDE ASSOCIATION STUDY; METABOLISM; METHYLATION; PROCEDURES; STATISTICS AND NUMERICAL DATA;

BIOMARKERS, TUMOR; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, LEUKEMIC; GENE ONTOLOGY; GENETIC HETEROGENEITY; GENOME-WIDE ASSOCIATION STUDY; HISTONES; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; METHYLATION; MODELS, GENETIC; PROMOTER REGIONS, GENETIC;

EID: 85009062830     PISSN: 14739542     EISSN: 14797364     Source Type: Journal    
DOI: 10.1186/s40246-016-0071-5     Document Type: Article

References (63)

1. Feinberg AP, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature. 1983;301(5895):89-92.
2. Cadieux B, Ching TT, VandenBerg SR, Costello JF. Genome-wide hypomethylation in human glioblastomas associated with specific copy number alteration, methylenetetrahydrofolate reductase allele status, and increased proliferation. Cancer Res. 2006;66(17):8469-76. doi:10.1158/0008- 5472.CAN-06-1547.
3. Widschwendter M, Jiang G, Woods C, Muller HM, Fiegl H, Goebel G, et al. DNA hypomethylation and ovarian cancer biology. Cancer Res. 2004;64 (13):4472-80. doi:10.1158/0008-5472.CAN-04-0238.
4. Brothman AR, Swanson G, Maxwell TM, Cui J, Murphy KJ, Herrick J, et al. Global hypomethylation is common in prostate cancer cells: a quantitative predictor for clinical outcome? Cancer Genet Cytogenet. 2005;156(1):31-6. doi:10.1016/j.cancergencyto.2004.04.004.
5. Wahlfors J, Hiltunen H, Heinonen K, Hamalainen E, Alhonen L, Janne J. Genomic hypomethylation in human chronic lymphocytic leukemia. Blood. 1992;80(8):2074-80.
6. Kulis M, Heath S, Bibikova M, Queiros AC, Navarro A, Clot G, et al. Epigenomic analysis detects widespread gene-body DNA hypomethylation in chronic lymphocytic leukemia. Nat Genet. 2012;44(11):1236-42. doi:10.1038/ng.2443.
7. Lin CH, Hsieh SY, Sheen IS, Lee WC, Chen TC, Shyu WC, et al. Genome-wide hypomethylation in hepatocellular carcinogenesis. Cancer Res. 2001;61(10): 4238-43.
8. Kim YI, Giuliano A, Hatch KD, Schneider A, Nour MA, Dallal GE, et al. Global DNA hypomethylation increases progressively in cervical dysplasia and carcinoma. Cancer. 1994;74(3):893-9.
9. Feinberg AP, Gehrke CW, Kuo KC, Ehrlich M. Reduced genomic 5- methylcytosine content in human colonic neoplasia. Cancer Res. 1988;48 (5):1159-61.
10. Ehrlich M, Jiang G, Fiala E, Dome JS, Yu MC, Long TI, et al. Hypomethylation and hypermethylation of DNA in Wilms tumors. Oncogene. 2002;21(43): 6694-702. doi:10.1038/sj.onc.1205890.
11. De Smet C, Lurquin C, Lethe B, Martelange V, Boon T. DNA methylation is the primary silencing mechanism for a set of germ line- and tumor-specific genes with a CpG-rich promoter. Mol Cell Biol. 1999;19(11):7327-35.
12. Li M, Balch C, Montgomery JS, Jeong M, Chung JH, Yan P, et al. Integrated analysis of DNA methylation and gene expression reveals specific signaling pathways associated with platinum resistance in ovarian cancer. BMC Med Genet. 2009;2:34. doi:10.1186/1755-8794-2-34.
13. Pulukuri SM, Estes N, Patel J, Rao JS. Demethylation-linked activation of urokinase plasminogen activator is involved in progression of prostate cancer. Cancer Res. 2007;67(3):930-9. doi:10.1158/0008-5472.can-06-2892.
14. Jackson K, Yu MC, Arakawa K, Fiala E, Youn B, Fiegl H, et al. DNA hypomethylation is prevalent even in low-grade breast cancers. Cancer Biol Ther. 2004;3(12):1225-31.
15. Ateeq B, Unterberger A, Szyf M, Rabbani SA. Pharmacological inhibition of DNA methylation induces proinvasive and prometastatic genes in vitro and in vivo. Neoplasia (New York, NY). 2008;10(3):266-78.
16. Denda A, Rao PM, Rajalakshmi S, Sarma DS. 5-azacytidine potentiates initiation induced by carcinogens in rat liver. Carcinogenesis. 1985;6(1):145-6.
17. Qu G, Dubeau L, Narayan A, Yu MC, Ehrlich M. Satellite DNA hypomethylation vs. overall genomic hypomethylation in ovarian epithelial tumors of different malignant potential. Mutat Res. 1999;423(1-2):91-101.
18. Rodriguez J, Vives L, Jorda M, Morales C, Munoz M, Vendrell E, et al. Genome-wide tracking of unmethylated DNA Alu repeats in normal and cancer cells. Nucleic Acids Res. 2008;36(3):770-84. doi:10.1093/nar/gkm1105.
19. Su M, Han D, Boyd-Kirkup J, Yu X, Han JD. Evolution of Alu elements toward enhancers. Cell Rep. 2014;7(2):376-85. doi:10.1016/j.celrep.2014.03.011.
20. Gribben JG. How I treat CLL up front. Blood. 2010;115(2):187-97. doi:10. 1182/blood-2009-08-207126.
21. Crespo M, Bosch F, Villamor N, Bellosillo B, Colomer D, Rozman M, et al. ZAP-70 expression as a surrogate for immunoglobulin-variable-region mutations in chronic lymphocytic leukemia. N Engl J Med. 2003;348(18): 1764-75. doi:10.1056/NEJMoa023143.
22. Damle RN, Wasil T, Fais F, Ghiotto F, Valetto A, Allen SL, et al. Ig V gene mutation status and CD38 expression as novel prognostic indicators in chronic lymphocytic leukemia. Blood. 1999;94(6):1840-7.
23. Hamblin TJ, Davis Z, Gardiner A, Oscier DG, Stevenson FK. Unmutated Ig V(H) genes are associated with a more aggressive form of chronic lymphocytic leukemia. Blood. 1999;94(6):1848-54.
24. Kanduri M, Cahill N, Goransson H, Enstrom C, Ryan F, Isaksson A, et al. Differential genome-wide array-based methylation profiles in prognostic subsets of chronic lymphocytic leukemia. Blood. 2010;115(2):296-305. doi:10. 1182/blood-2009-07-232868.
25. Rush LJ, Raval A, Funchain P, Johnson AJ, Smith L, Lucas DM, et al. Epigenetic profiling in chronic lymphocytic leukemia reveals novel methylation targets. Cancer Res. 2004;64(7):2424-33.
26. Raval A, Tanner SM, Byrd JC, Angerman EB, Perko JD, Chen SS, et al. Downregulation of death-associated protein kinase 1 (DAPK1) in chronic lymphocytic leukemia. Cell. 2007;129(5):879-90. doi:10.1016/j.cell.2007.03.043.
27. Liu TH, Raval A, Chen SS, Matkovic JJ, Byrd JC, Plass C. CpG island methylation and expression of the secreted frizzled-related protein gene family in chronic lymphocytic leukemia. Cancer Res. 2006;66(2):653-8. doi: 10.1158/0008-5472.can-05-3712.
28. Chen SS, Claus R, Lucas DM, Yu L, Qian J, Ruppert AS, et al. Silencing of the inhibitor of DNA binding protein 4 (ID4) contributes to the pathogenesis of mouse and human CLL. Blood. 2011;117(3):862-71. doi:10.1182/blood-2010- 05-284638.
29. Seeliger B, Wilop S, Osieka R, Galm O, Jost E. CpG island methylation patterns in chronic lymphocytic leukemia. Leuk Lymphoma. 2009;50(3):419-26. doi:10.1080/10428190902756594.
30. Raval A, Lucas DM, Matkovic JJ, Bennett KL, Liyanarachchi S, Young DC, et al. TWIST2 demonstrates differential methylation in immunoglobulin variable heavy chain mutated and unmutated chronic lymphocytic leukemia. J Clin Oncol Off J Am Soc Clin Oncol. 2005;23(17):3877-85. doi:10.1200/jco.2005.02.196.
31. Lipsanen V, Leinonen P, Alhonen L, Janne J. Hypomethylation of ornithine decarboxylase gene and erb-A1 oncogene in human chronic lymphatic leukemia. Blood. 1988;72(6):2042-4.
32. Hanada M, Delia D, Aiello A, Stadtmauer E, Reed JC. bcl-2 gene hypomethylation and high-level expression in B-cell chronic lymphocytic leukemia. Blood. 1993;82(6):1820-8.
33. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature. 2011;473(7345):43-9. doi:10.1038/nature09906.
34. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25(1):25-9. doi:10.1038/75556.
35. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M. KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res. 2010;38(Database issue):D355-60. doi:10.1093/nar/ gkp896.
36. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, et al. Identification and analysis of functional elements in 1 % of the human genome by the ENCODE pilot project. Nature. 2007;447(7146):799-816. doi:10.1038/nature05874.
37. Filion GJ, Zhenilo S, Salozhin S, Yamada D, Prokhortchouk E, Defossez PA. A family of human zinc finger proteins that bind methylated DNA and repress transcription. Mol Cell Biol. 2006;26(1):169-81. doi:10.1128/mcb.26.1.169-181.2006.
38. Hogart A, Lichtenberg J, Ajay SS, Anderson S, Margulies EH, Bodine DM. Genome-wide DNA methylation profiles in hematopoietic stem and progenitor cells reveal overrepresentation of ETS transcription factor binding sites. Genome Res. 2012;22(8):1407-18. doi:10.1101/gr.132878.111.
39. Miller DM, Thomas SD, Islam A, Muench D, Sedoris K. c-Myc and cancer metabolism. Clin Cancer Res. 2012;18(20):5546-53. doi:10.1158/1078-0432. ccr-12-0977.
40. Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinf. 2008;9:559. doi:10.1186/1471-2105-9-559.
41. Chiorazzi N, Ferrarini M. B cell chronic lymphocytic leukemia: lessons learned from studies of the B cell antigen receptor. Annu Rev Immunol. 2003;21:841-94. doi:10.1146/annurev.immunol.21.120601.141018.
42. Hagman J, Ramirez J, Lukin K. B lymphocyte lineage specification, commitment and epigenetic control of transcription by early B cell factor 1. Curr Top Microbiol Immunol. 2012;356:17-38. doi:10.1007/82-2011-139.
43. Robertson AG, Bilenky M, Tam A, Zhao Y, Zeng T, Thiessen N, et al. Genome-wide relationship between histone H3 lysine 4 mono- and trimethylation and transcription factor binding. Genome Res. 2008;18(12): 1906-17. doi:10.1101/gr.078519.108.
44. Hazan RB, Qiao R, Keren R, Badano I, Suyama K. Cadherin switch in tumor progression. Ann N Y Acad Sci. 2004;1014:155-63.
45. Tsurimoto T, Shinozaki A, Yano M, Seki M, Enomoto T. Human Werner helicase interacting protein 1 (WRNIP1) functions as a novel modulator for DNA polymerase delta. Genes to cells : devoted to molecular and cellular mechanisms. 2005;10(1):13-22. doi:10.1111/j.1365-2443.2004.00812.x.
46. Yoon HG, Chan DW, Huang ZQ, Li J, Fondell JD, Qin J, et al. Purification and functional characterization of the human N-CoR complex: the roles of HDAC3, TBL1 and TBLR1. The EMBO journal. 2003;22(6):1336-46. doi:10. 1093/emboj/cdg120.
47. Kashatus D, Cogswell P, Baldwin AS. Expression of the Bcl-3 proto-oncogene suppresses p53 activation. Genes Dev. 2006;20(2):225-35. doi:10.1101/gad.1352206.
48. Massoumi R, Chmielarska K, Hennecke K, Pfeifer A, Fassler R. Cyld inhibits tumor cell proliferation by blocking Bcl-3-dependent NF-kappaB signaling. Cell. 2006;125(4):665-77. doi:10.1016/j.cell.2006.03.041.
49. Fu H, Maunakea AK, Martin MM, Huang L, Zhang Y, Ryan M, et al. Methylation of histone H3 on lysine 79 associates with a group of replication origins and helps limit DNA replication once per cell cycle. PLoS Genet. 2013;9(6), e1003542. doi:10.1371/journal.pgen.1003542.
50. Sims 3rd RJ, Reinberg D. Processing the H3K36me3 signature. Nat Genet. 2009;41(3):270-1. doi:10.1038/ng0309-270.
51. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science. 2002;298(5595):1039-43. doi:10.1126/science.1076997.
52. Reddington JP, Perricone SM, Nestor CE, Reichmann J, Youngson NA, Suzuki M, et al. Redistribution of H3K27me3 upon DNA hypomethylation results in de-repression of Polycomb target genes. Genome Biol. 2013;14(3):R25. doi: 10.1186/gb-2013-14-3-r25.
53. Ng SY, Yoshida T, Zhang J, Georgopoulos K. Genome-wide lineage-specific transcriptional networks underscore Ikaros-dependent lymphoid priming in hematopoietic stem cells. Immunity. 2009;30(4):493-507. doi:10.1016/j. immuni.2009.01.014.
54. Fujita T, Nolan GP, Liou HC, Scott ML, Baltimore D. The candidate protooncogene bcl-3 encodes a transcriptional coactivator that activates through NF-kappa B p50 homodimers. Genes Dev. 1993;7(7B):1354-63.
55. Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics (Oxford, England). 2011;27(11): 1571-2. doi:10.1093/bioinformatics/btr167.
56. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28(5):511-5. doi:10.1038/nbt.1621.
57. Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol. 2013;31(1):46-53. doi:10.1038/nbt.2450.
58. Akalin A, Kormaksson M, Li S, Garrett-Bakelman FE, Figueroa ME, Melnick A, et al. methylKit: a comprehensive R package for the analysis of genomewide DNA methylation profiles. Genome Biol. 2012;13(10):R87. doi:10.1186/ gb-2012-13-10-r87.
59. Falcon S, Gentleman R. Using GOstats to test gene lists for GO term association. Bioinformatics (Oxford, England). 2007;23(2):257-8. doi:10.1093/ bioinformatics/btl567.
60. Stelzer G, Inger A, Olender T, Iny-Stein T, Dalah I, Harel A, et al. GeneDecks: paralog hunting and gene-set distillation with GeneCards annotation. OMICS. 2009;13(6):477-87. doi:10.1089/omi.2009.0069.
61. Dozmorov MG, Cara LR, Giles CB, Wren JD. GenomeRunner: automating genome exploration. Bioinformatics (Oxford, England). 2012;28(3):419-20. doi:10.1093/bioinformatics/btr666.
62. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, et al. Simple combinations of lineage-determining transcription factors prime cisregulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38(4):576-89. doi:10.1016/j.molcel.2010.05.004.
63. Langfelder P, Luo R, Oldham MC, Horvath S. Is my network module preserved and reproducible? PLoS Comput Biol. 2011;7(1), e1001057. doi:10. 1371/journal.pcbi.1001057.