Genome-wide characterization of cytosine-specific 5-hydroxymethylation in normal breast tissue

References

• Tahiliani M, Koh KP, Shen Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 2009;324:930–935.
   PubMed Web of Science ®Google Scholar
• Yi C, Yang C-G, He C. A non-heme iron-mediated chemical demethylation in DNA and RNA. Acc Chem Res. 2009;42:519–529.
   PubMed Web of Science ®Google Scholar
• Wu X, Zhang Y. TET-mediated active DNA demethylation: mechanism, function and beyond. Nat Rev Genet. 2017;18:517–534.
   PubMed Web of Science ®Google Scholar
• Ito S, Shen L, Dai Q, et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science. 2011;333:1300–1303.
   PubMed Web of Science ®Google Scholar
• Bachman M, Uribe-Lewis S, Yang X, et al. 5-Hydroxymethylcytosine is a predominantly stable DNA modification. Nat Chem. 2014;6:1049–1055.
   PubMed Web of Science ®Google Scholar
• Branco MR, Ficz G, Reik W. Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat Rev Genet. 2011;13:7–13.
   PubMed Web of Science ®Google Scholar
• Stroud H, Feng S, Morey Kinney S, et al. 5-Hydroxymethylcytosine is associated with enhancers and gene bodies in human embryonic stem cells. Genome Biol. 2011;12:R54.
   PubMed Web of Science ®Google Scholar
• Yu M, Hon GC, Szulwach KE, et al. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell. 2012;149:1368–1380.
   PubMed Web of Science ®Google Scholar
• Sun Z, Dai N, Borgaro JG, et al. A sensitive approach to map genome-wide 5-hydroxymethylcytosine and 5-formylcytosine at single-base resolution. Mol Cell. 2015;57:750–761.
   PubMed Web of Science ®Google Scholar
• Pastor WA, Pape UJ, Huang Y, et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature. 2011;473:394–397.
   PubMed Web of Science ®Google Scholar
• Ficz G, Branco MR, Seisenberger S, et al. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature. 2011;473:398–402.
   PubMed Web of Science ®Google Scholar
• Wen L, Li X, Yan L, et al. Whole-genome analysis of 5-hydroxymethylcytosine and 5-methylcytosine at base resolution in the human brain. Genome Biol. 2014;15:R49.
   PubMed Web of Science ®Google Scholar
• Iurlaro M, Ficz G, Oxley D, et al. A screen for hydroxymethylcytosine and formylcytosine binding proteins suggests functions in transcription and chromatin regulation. Genome Biol. 2013;14:R119.
   PubMed Web of Science ®Google Scholar
• Spruijt CG, Gnerlich F, Smits AH, et al. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell. 2013;152:1146–1159.
   PubMed Web of Science ®Google Scholar
• Mellen M, Ayata P, Dewell S, et al. MeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system. Cell. 2012;151:1417–1430.
   PubMed Web of Science ®Google Scholar
• Yildirim O, Li R, Hung J-H, et al. Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells. Cell. 2011;147:1498–1510.
   PubMed Web of Science ®Google Scholar
• Zhong J, Li X, Cai W, et al. TET1 modulates H4K16 acetylation by controlling auto-acetylation of hMOF to affect gene regulation and DNA repair function. Nucleic Acids Res. 2017;45:672–684.
   PubMed Web of Science ®Google Scholar
• Kafer GR, Li X, Horii T, et al. 5-Hydroxymethylcytosine marks sites of DNA damage and promotes genome stability. Cell Rep. 2016;14:1283–1292.
   PubMed Web of Science ®Google Scholar
• Nestor CE, Ottaviano R, Reddington J, et al. Tissue type is a major modifier of the 5-hydroxymethylcytosine content of human genes. Genome Res. 2012;22:467–477.
   PubMed Web of Science ®Google Scholar
• Kriaucionis S, Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science. 2009;324:929–930.
   PubMed Web of Science ®Google Scholar
• Jin S-G, Wu X, Li AX, et al. Genomic mapping of 5-hydroxymethylcytosine in the human brain. Nucleic Acids Res. 2011;39:5015–5024.
   PubMed Web of Science ®Google Scholar
• Guo JU, Su Y, Zhong C, et al. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell. 2011;145:423–434.
   PubMed Web of Science ®Google Scholar
• Song C-X, Szulwach KE, Fu Y, et al. Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat Biotechnol. 2011;29:68–72.
   PubMed Web of Science ®Google Scholar
• Lunnon K, Hannon E, Smith RG, et al. Variation in 5-hydroxymethylcytosine across human cortex and cerebellum. Genome Biol. 2016;17:27.
   PubMed Web of Science ®Google Scholar
• Szulwach KE, Li X, Li Y, et al. 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat Neurosci. 2011;14:1607–1616.
   PubMed Web of Science ®Google Scholar
• Vasanthakumar A, Godley LA. 5-hydroxymethylcytosine in cancer: significance in diagnosis and therapy. Cancer Genet. 2015;208:167–177.
   PubMed Web of Science ®Google Scholar
• Jin S-G, Jiang Y, Qiu R, et al. 5-Hydroxymethylcytosine is strongly depleted in human cancers but its levels do not correlate with IDH1 mutations. Cancer Res. 2011;71:7360–7365.
   PubMed Web of Science ®Google Scholar
• Kudo Y, Tateishi K, Yamamoto K, et al. Loss of 5-hydroxymethylcytosine is accompanied with malignant cellular transformation. Cancer Sci. 2012;103:670–676.
   PubMed Web of Science ®Google Scholar
• Jin C, Lu Y, Jelinek J, et al. TET1 is a maintenance DNA demethylase that prevents methylation spreading in differentiated cells. Nucleic Acids Res. 2014;42:6956–6971.
   PubMed Web of Science ®Google Scholar
• Skvortsova K, Masle-Farquhar E, Luu P-L, et al. DNA hypermethylation encroachment at CpG island borders in cancer is predisposed by H3K4 monomethylation patterns. Cancer Cell. 2019;35:297–314.e8.
   PubMed Web of Science ®Google Scholar
• Song SJ, Poliseno L, Song MS, et al. MicroRNA-antagonism regulates breast cancer stemness and metastasis via TET-family-dependent chromatin remodeling. Cell. 2013;154:311–324.
   PubMed Web of Science ®Google Scholar
• Thienpont B, Steinbacher J, Zhao H, et al. Tumour hypoxia causes DNA hypermethylation by reducing TET activity. Nature. 2016;537:63–68.
   PubMed Web of Science ®Google Scholar
• Li L, Li C, Mao H, et al. Epigenetic inactivation of the CpG demethylase TET1 as a DNA methylation feedback loop in human cancers. Sci Rep. 2016;6:26591.
   PubMed Web of Science ®Google Scholar
• Yamazaki J, Jelinek J, Lu Y, et al. TET2 Mutations Affect Non-CpG Island DNA Methylation at Enhancers and Transcription Factor-Binding Sites in Chronic Myelomonocytic Leukemia. Cancer Res. 2015;75:2833–2843.
   PubMed Web of Science ®Google Scholar
• Rampal R, Alkalin A, Madzo J, et al. DNA hydroxymethylation profiling reveals that WT1 mutations result in loss of TET2 function in acute myeloid leukemia. Cell Rep. 2014;9:1841–1855.
   PubMed Web of Science ®Google Scholar
• Fleischer T, Frigessi A, Johnson KC, et al. Genome-wide DNA methylation profiles in progression to in situ and invasive carcinoma of the breast with impact on gene transcription and prognosis. Genome Biol. 2014;15:435.
   PubMed Web of Science ®Google Scholar
• Johnson KC, Koestler DC, Fleischer T, et al. DNA methylation in ductal carcinoma in situ related with future development of invasive breast cancer. Clin Epigenetics. 2015;7:75.
   PubMed Web of Science ®Google Scholar
• Tsai K-W, Li G-C, Chen C-H, et al. Reduction of global 5-hydroxymethylcytosine is a poor prognostic factor in breast cancer patients, especially for an ER/PR-negative subtype. Breast Cancer Res Treat. 2015;153:219–234.
   PubMed Web of Science ®Google Scholar
• Booth MJ, Branco MR, Ficz G, et al. Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science. 2012;336:934–937.
   PubMed Web of Science ®Google Scholar
• Booth MJ, Ost TWB, Beraldi D, et al. Oxidative bisulfite sequencing of 5-methylcytosine and 5-hydroxymethylcytosine. Nat Protoc. 2013;8:1841–1851.
   PubMed Web of Science ®Google Scholar
• Field SF, Beraldi D, Bachman M, et al. Accurate measurement of 5-methylcytosine and 5-hydroxymethylcytosine in human cerebellum DNA by oxidative bisulfite on an array (OxBS-array). PLoS One. 2015;10:e0118202.
   PubMed Web of Science ®Google Scholar
• Stewart SK, Morris TJ, Guilhamon P, et al. oxBS-450K: a method for analysing hydroxymethylation using 450K bead chips. Methods. 2015;72:9–15.
   PubMed Web of Science ®Google Scholar
• Johnson KC, Houseman EA, King JE, et al. 5-Hydroxymethylcytosine localizes to enhancer elements and is associated with survival in glioblastoma patients. Nat Commun. 2016;7:13177.
   PubMed Web of Science ®Google Scholar
• Green BB, Houseman EA, Johnson KC, et al. Hydroxymethylation is uniquely distributed within term placenta, and is associated with gene expression. Faseb J. 2016;30:2874–2884.
   PubMed Web of Science ®Google Scholar
• Houseman EA, Johnson KC, Christensen BC. OxyBS: estimation of 5-methylcytosine and 5-hydroxymethylcytosine from tandem-treated oxidative bisulfite and bisulfite DNA. Bioinformatics. 2016;32:2505–2507.
   PubMed Web of Science ®Google Scholar
• Jaffe AE, Irizarry RA. Accounting for cellular heterogeneity is critical in epigenome-wide association studies. Genome Biol. 2014;15:R31.
   PubMed Web of Science ®Google Scholar
• Houseman EA, Molitor J, Marsit CJ. Reference-free cell mixture adjustments in analysis of DNA methylation data. Bioinformatics. 2014;30:1431–1439.
   PubMed Web of Science ®Google Scholar
• Mostowy S, Cossart P. Septins: the fourth component of the cytoskeleton. Nat Rev Mol Cell Biol. 2012;13:183–194.
   PubMed Web of Science ®Google Scholar
• Wu H, D’Alessio AC, Ito S, et al. Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev. 2011;25:679–684.
   PubMed Web of Science ®Google Scholar
• Bernstein BE, Stamatoyannopoulos JA, Costello JF, et al. The NIH roadmap epigenomics mapping consortium. Nat Biotechnol. 2010;28:1045–1048.
   PubMed Web of Science ®Google Scholar
• Roadmap Epigenomics C, Kundaje A, Meuleman W, et al. Integrative analysis of 111 reference human epigenomes. Nature. 2015;518:317–330.
   PubMed Web of Science ®Google Scholar
• McLean CY, Bristor D, Hiller M, et al. GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol. 2010;28:495–501.
   PubMed Web of Science ®Google Scholar
• Iliopoulos D, Hirsch HA, Struhl K. An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell. 2009;139:693–706.
   PubMed Web of Science ®Google Scholar
• Kroeze LI, van der Reijden BA, Jansen JH. 5-Hydroxymethylcytosine: an epigenetic mark frequently deregulated in cancer. Biochim Biophys Acta. 2015;1855:144–154.
   PubMed Web of Science ®Google Scholar
• Lian CG, Xu Y, Ceol C, et al. Loss of 5-hydroxymethylcytosine is an epigenetic hallmark of melanoma. Cell. 2012;150:1135–1146.
   PubMed Web of Science ®Google Scholar
• Bachman M, Uribe-Lewis S, Yang X, et al. 5-Formylcytosine can be a stable DNA modification in mammals. Nat Chem Biol. 2015;11:555–557.
   PubMed Web of Science ®Google Scholar
• Doege CA, Inoue K, Yamashita T, et al. Early-stage epigenetic modification during somatic cell reprogramming by Parp1 and Tet2. Nature. 2012;488:652–655.
   PubMed Web of Science ®Google Scholar
• Hu X, Zhang L, Mao S-Q, et al. Tet and TDG mediate DNA demethylation essential for mesenchymal-to-epithelial transition in somatic cell reprogramming. Cell Stem Cell. 2014;14:512–522.
   PubMed Web of Science ®Google Scholar
• Lio C-W, Zhang J, Gonzalez-Avalos E, et al. Tet2 and Tet3 cooperate with B-lineage transcription factors to regulate DNA modification and chromatin accessibility. Elife. 2016;5:e18290.
   Web of Science ®Google Scholar
• Wheldon LM, Abakir A, Ferjentsik Z, et al. Transient accumulation of 5-carboxylcytosine indicates involvement of active demethylation in lineage specification of neural stem cells. Cell Rep. 2014;7:1353–1361.
   PubMed Web of Science ®Google Scholar
• Yue X, Trifari S, Aijo T, et al. Control of Foxp3 stability through modulation of TET activity. J Exp Med. 2016;213:377–397.
   PubMed Web of Science ®Google Scholar
• Orlanski S, Labi V, Reizel Y, et al. Tissue-specific DNA demethylation is required for proper B-cell differentiation and function. Proc Natl Acad Sci U S A. 2016;113:5018–5023.
   PubMed Web of Science ®Google Scholar
• Xu Y, Wu F, Tan L, et al. Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Mol Cell. 2011;42:451–464.
   PubMed Web of Science ®Google Scholar
• Chuong EB, Elde NC, Feschotte C. Regulatory activities of transposable elements: from conflicts to benefits. Nat Rev Genet. 2017;18:71–86.
   PubMed Web of Science ®Google Scholar
• Haffner MC, Chaux A, Meeker AK, et al. Global 5-hydroxymethylcytosine content is significantly reduced in tissue stem/progenitor cell compartments and in human cancers. Oncotarget. 2011;2:627–637.
   PubMed Web of Science ®Google Scholar
• Robertson KD. DNA methylation, methyltransferases, and cancer. Oncogene. 2001;20:3139–3155.
   PubMed Web of Science ®Google Scholar
• Ehrlich M. DNA hypomethylation in cancer cells. Epigenomics. 2009;1:239–259.
   PubMed Web of Science ®Google Scholar
• Bhattacharyya S, Pradhan K, Campbell N, et al. Altered hydroxymethylation is seen at regulatory regions in pancreatic cancer and regulates oncogenic pathways. Genome Res. 2017;27:1830–1842.
   PubMed Web of Science ®Google Scholar
• Takai H, Masuda K, Sato T, et al. 5-Hydroxymethylcytosine plays a critical role in glioblastomagenesis by recruiting the CHTOP-methylosome complex. Cell Rep. 2014;9:48–60.
   PubMed Web of Science ®Google Scholar
• Wu M-Z, Chen S-F, Nieh S, et al. Hypoxia Drives Breast Tumor Malignancy through a TET-TNFalpha-p38-MAPK Signaling Axis. Cancer Res. 2015;75:3912–3924.
   PubMed Web of Science ®Google Scholar
• Connolly D, Abdesselam I, Verdier-Pinard P, et al. Septin roles in tumorigenesis. Biol Chem. 2011;392:725–738.
   PubMed Web of Science ®Google Scholar
• Montagna C, Lyu MS, Hunter K, et al. The Septin 9 (MSF) gene is amplified and overexpressed in mouse mammary gland adenocarcinomas and human breast cancer cell lines. Cancer Res. 2003;63:2179–2187.
   PubMed Web of Science ®Google Scholar
• Connolly D, Yang Z, Castaldi M, et al. Septin 9 isoform expression, localization and epigenetic changes during human and mouse breast cancer progression. Breast Cancer Res. 2011;13:R76.
   PubMed Web of Science ®Google Scholar
• Connolly D, Hoang HG, Adler E, et al. Septin 9 amplification and isoform-specific expression in peritumoral and tumor breast tissue. Biol Chem. 2014;395:157–167.
   PubMed Web of Science ®Google Scholar
• Verdier-Pinard P, Salaun D, Bouguenina H, et al. Septin 9_i2 is downregulated in tumors, impairs cancer cell migration and alters subnuclear actin filaments. Sci Rep. 2017;7:44976.
   PubMed Web of Science ®Google Scholar
• Potter NT, Hurban P, White MN, et al. Validation of a real-time PCR-based qualitative assay for the detection of methylated SEPT9 DNA in human plasma. Clin Chem. 2014;60:1183–1191.
   PubMed Web of Science ®Google Scholar
• Matsui S, Kagara N, Mishima C, et al. Methylation of the SEPT9_v2 promoter as a novel marker for the detection of circulating tumor DNA in breast cancer patients. Oncol Rep. 2016;36:2225–2235.
   PubMed Web of Science ®Google Scholar
• Ross-Innes CS, Stark R, Teschendorff AE, et al. Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature. 2012;481:389–393.
   PubMed Web of Science ®Google Scholar
• Hurtado A, Holmes KA, Ross-Innes CS, et al. FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat Genet. 2011;43:27–33.
   PubMed Web of Science ®Google Scholar
• Theodorou V, Stark R, Menon S, et al. GATA3 acts upstream of FOXA1 in mediating ESR1 binding by shaping enhancer accessibility. Genome Res. 2013;23:12–22.
   PubMed Web of Science ®Google Scholar
• Hua S, Kittler R, White KP. Genomic antagonism between retinoic acid and estrogen signaling in breast cancer. Cell. 2009;137:1259–1271.
   PubMed Web of Science ®Google Scholar
• Yang H, Liu Y, Bai F, et al. Tumor development is associated with decrease of TET gene expression and 5-methylcytosine hydroxylation. Oncogene. 2013;32:663–669.
   PubMed Web of Science ®Google Scholar
• Hsu C-H, Peng K-L, Kang M-L, et al. TET1 suppresses cancer invasion by activating the tissue inhibitors of metalloproteinases. Cell Rep. 2012;2:568–579.
   PubMed Web of Science ®Google Scholar
• Good CR, Panjarian S, Kelly AD, et al. TET1-mediated hypomethylation activates oncogenic signaling in triple-negative breast cancer. Cancer Res. 2018;78:4126–4137.
   PubMed Web of Science ®Google Scholar
• Bibikova M, Barnes B, Tsan C, et al. High density DNA methylation array with single CpG site resolution. Genomics. 2011;98:288–295.
   PubMed Web of Science ®Google Scholar
• Zheng Y, Joyce BT, Liu L, et al. Prediction of genome-wide DNA methylation in repetitive elements. Nucleic Acids Res. 2017;45:8697–8711.
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas N. Comprehensive molecular portraits of human breast tumours. Nature. 2012;490:61–70.
   PubMed Web of Science ®Google Scholar
• Colaprico A, Silva TC, Olsen C, et al. TCGAbiolinks: an R/Bioconductor package for integrative analysis of TCGA data. Nucleic Acids Res. 2016;44:e71.
   PubMed Web of Science ®Google Scholar
• Irizarry RA, Ladd-Acosta C, Wen B, et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet. 2009;41:178–186.
   PubMed Web of Science ®Google Scholar
• Sandoval J, Heyn H, Moran S, et al. Validation of a DNA methylation microarray for 450,000 CpG sites in the human genome. Epigenetics. 2011;6:692–702.
   PubMed Web of Science ®Google Scholar
• Smit A, Hubley R, Green P. RepeatMasker open-4.0. 2013–2015. Available from: http://wwwrepeatmaskerorg
   Google Scholar
• Durinck S, Spellman PT, Birney E, et al. Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt. Nat Protoc. 2009;4:1184–1191.
   PubMed Web of Science ®Google Scholar
• Salas LA, Johnson KC, Koestler DC, et al. Integrative epigenetic and genetic pan-cancer somatic alteration portraits. Epigenetics. 2017;12:561–574.
   PubMed Web of Science ®Google Scholar
• Assenov Y, Muller F, Lutsik P, et al. Comprehensive analysis of DNA methylation data with RnBeads. Nat Methods. 2014;11:1138–1140.
   PubMed Web of Science ®Google Scholar
• Du P, Zhang X, Huang CC, et al. Comparison of Beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics. 2010;11:587.
   PubMed Web of Science ®Google Scholar
• Triche TJ Jr., Weisenberger DJ, Van Den Berg D, et al. Low-level processing of illumina infinium DNA methylation bead arrays. Nucleic Acids Res. 2013;41:e90.
   PubMed Web of Science ®Google Scholar
• Fortin JP, Labbe A, Lemire M, et al. Functional normalization of 450k methylation array data improves replication in large cancer studies. Genome Biol. 2014;15:503.
   PubMed Web of Science ®Google Scholar
• Chen YA, Lemire M, Choufani S, et al. Discovery of cross-reactive probes and polymorphic CpGs in the illumina infinium human Methylation450 microarray. Epigenetics. 2013;8:203–209.
   PubMed Web of Science ®Google Scholar
• Ritchie ME, Phipson B, Wu D, et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43:e47.
   PubMed Web of Science ®Google Scholar
• Houseman EA, Accomando WP, Koestler DC, et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics. 2012;13:86.
   PubMed Web of Science ®Google Scholar
• Houseman EA, Kelsey KT, Wiencke JK, et al. Cell-composition effects in the analysis of DNA methylation array data: a mathematical perspective. BMC Bioinformatics. 2015;16:95.
   PubMed Web of Science ®Google Scholar
• Titus AJ, Gallimore RM, Salas LA, et al. Cell-type deconvolution from DNA methylation: a review of recent applications. Hum Mol Genet. 2017;26:R216–R24.
   PubMed Web of Science ®Google Scholar