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DNA methylation data for identification of epigenetic targets of resveratrol in triple negative breast cancer cells
Data in Brief 11 (2017) 169–182
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DNA methylation data for identification of epigenetic targets of resveratrol in triple negative breast cancer cells Rubiceli Medina-Aguilar a, Carlos Pérez-Plasencia b, Patricio Gariglio a, Laurence A. Marchat c, Ali Flores-Pérez d, César López-Camarillo d,n, Jaime García Mena a,n a Departmento de Genética y Biología Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (Cinvestav-IPN), México City, México b Unidad de Biomedicina, FES-Iztacala UNAM, Tlalnepantla, Estado de México, México c Escuela Nacional de Medicina y Homeopatía. Red de Biotecnología. Instituto Politécnico Nacional, México City, México d Laboratorio de Oncogenómica y Proteómica del Cáncer, Universidad Autónoma de la Ciudad de México, México City, México
a r t i c l e i n f o
abstract
Article history: Received 2 November 2016 Received in revised form 6 January 2017 Accepted 2 February 2017 Available online 9 February 2017
Previous studies revealed that some bioactive food components have anti-cancer effects. However epigenetic effects of dietary compound resveratrol are largely unknown in breast cancer cells (M.A. Dawson, T. Kouzarides, 2012) [1]. Here we provide novel data and comparisons of DNA methylation status of promoter gene regions in response to resveratrol treatment at 24 h and 48 h versus untreated MDA-MB-231 breast cancer cells. DNA methylation changes were measured using Array-PRIMES method (aPRIMES) followed by whole-genome hybridization using human DNA methylation promoter microarray NimbleGen HG18 Refseq Promoter 3 720 K array. Our data were associated to corresponding changes in mRNA expression in a set of cancer-related genes. Using gene ontology analysis we also identify cancer-related cellular processes and pathways that can be epigenetically reprogramed by resveratrol. Data in this article are associated to the research articles “Methylation Landscape of Human Breast Cancer Cells in Response to Dietary Compound Resveratrol”. Medina Aguilar et al., PLoS ONE 11(6): e0157866. doi:10.1371/journal. pone.0157866 2016 (A.R. Medina, P.C. Pérez, L.A. Marchat, P.
Keywords: Breast cancer Resveratrol DNA methylation Oncogenes Tumor suppressor genes Genome-wide methylome
n
Corresponding authors. E-mail addresses: [email protected] (C. López-Camarillo), [email protected] (J. García Mena).
http://dx.doi.org/10.1016/j.dib.2017.02.006 2352-3409/& 2017 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
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Gariglio, M.J. García, C.S. Rodríguez, G.E. Ruíz, et al., 2016) [2]; and “Resveratrol inhibits cell cycle progression by targeting Aurora kinase A and Polo-like kinase 1 in breast cancer cells” in Oncology Reports. Medina Aguilar et al., 2016 Jun; 35(6):3696-704. doi: 10.3892/or.2016.4728 (A.R. Medina, P. Gariglio, M.J. García, O.E. Arechaga, S.N. Villegas, C.M. Martínez et al., 2016) [3]. & 2017 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Specifications Table Subject area More specific subject area Type of data How data was acquired Data format Experimental factors
Experimental features
Data source location Data accessibility
Biology Breast cancer, Epigenetics Tables, figure, raw data on DNA methylation (peak scores) Array-PRIMES method (aPRIMES). NimbleGen HG18 Refseq Promoter 3 720 K arrays. Filtered for peak annotation, and analyzed for differential enrichment and gene ontology DNA from untreated and treated MDA-MB-231 cells with resveratrol (100 mM) at 24 h and 48 h was extracted using the DNeasy Kit (Qiagen, Germany). To identify methylated and unmethylated DNA regions in the promoters of genes, we used Array-PRIMES method (aPRIMES). MDA-MB-231 cells were treated with resveratrol for 24 h and 48 h. For DNA methylation analysis we used NimbleGen HG18 Refseq Promoter 3 720 K array. The array covering 30,848 transcripts, 22,532 promoters, and 27,728 CpG islands. Oncogenomics and Cancer Proteomics Laboratory, UACM. México City, México. Data is available with this article.
Value of the data
First analysis on DNA methylation of promoter genes in triple negative breast cancer cells treated with resveratrol, spanning 27,728 CpG loci.
Provides genomic data indicating that resveratrol impacts the epigenetic landscape by changing DNA methylation status of specific oncogenes and tumor suppressor genes in breast cancer cells.
Analyses indicate that resveratrol epigenetically alters regulation of particular genes involved in cancer in triple negative breast cancer cells.
Data provided here serves as a novel and free resource for researchers working in the field of epigenetic regulation of cancer related genes in response to naturally occurring dietary compounds.
1. Data In this study we performed a genome-wide survey of DNA methylation in MDA-MB-231 triplenegative breast cancer cells exposed to resveratrol [1,3]. To determine the methylated and unmethylated DNA regions in the promoters of genes we used Array-PRIMES method (aPRIMES) [[4], Fig. 1]. The extensive annotation of peaks differentially enriched for DNA methylation and peak comparisons between the MDA-MB-231 breast cancer cells treated with resveratrol at 24 h and 48 h versus
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Fig. 1. Array-PRIMES procedure and NimbleGen HG18 Refseq Promoter 3 720 K arrays analysis. Genomic DNA (500 ng) was restricted to completion with MseI restriction enzyme. Then, DNA fragments produced by MseI were subjected to linkermediated PCR. Half of the resulting ligated MseI fragments were digested with McrBC restriction enzyme while the other half of MseI fragments was digested with the two methylation-sensitive endonucleases HpaII and BstUI. The experimental and control DNA was labeled with Cy3 and Cy5 nonamers. Methylated DNA fractions are highlighted in red and are expected to result in positive ratios and green spots indicate unmethylation and are to have negative ratios. DNA methylation analysis raw data was normalized and differential intensity of each probe compared with input control was calculated using the NimbleGen software DEVA. Average fold change (experimental IP sample versus Control input sample) in a range of 2.44 kb upstream and 610 bp downstream window from RefSeq transcription start sites (TSS). Modified from Pfister, S., Schlaeger, C., Mendrzyk, F., Wittmann, A., Benner, A., Kulozik, A., et al. Array-based profiling of reference-independent methylation status (aPRIMES) identifies frequent promoter methylation and consecutive downregulation of ZIC2 in pediatric medulloblastoma. Nucleic Acids Res. (2007) 35:e51.
untreated cells (Tables 1, and 2) were performed using the DEVA 1.2.1 software [2]. At 24 h treatment, 338 out of 2035 hypermethylated genes correspond to cancer genes; and 92 out of 1738 hypomethylated genes correspond to cancer genes. At 48 h treatment, 137 out of 1869 hypermethylated genes were cancer genes; and 288 out of 1661 hypomethylated genes are cancer genes (Tables 3 and 4). In addition, differentially methylated probes and differentially expressed genes were identified between the MDA-MB-231 cells treated with resveratrol at 24 h and 48 h and the MDA-MB-231 untreated. The integrative analysis of DNA methylation and gene expression at different times of resveratrol exposure showed that changes in DNA methylation were associated to corresponding changes in mRNA expression in a set of cancer-related genes (Tables 5 and 6).
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Table 1 Annotation of peak values indicating differentially enriched DNA methylation between the MDA-MB-231 breast cancer cells treated with resveratrol at 24 h versus non-treated cells. Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr8 chrX chr17 chr11 chr1 chr15 chr18 chr11 chr4 chr17 chr8 chr22 chr5 chr7 chr10 chr17 chr9 chr14 chr5 chr10 chr8 chr4 chr19 chr2 chr12 chr7 chr10 chr19 chr20 chr9 chr10 chr22 chr7 chr17 chr17 chr8 chr5 chr1 chr9 chr1 chr21 chr3 chr2 chr6 chr2 chr1 chr20 chr2 chr3 chr10 chr20 chr5 chr9 chr12 chr4 chr22 chr12 chr5
1784829 1521952 60265001 125641836 228481793 98649690 74927964 2941097 2703310 13340300 6411612 18274404 1536587 154718039 120791601 77869583 115101938 104982606 140747519 105835961 145642211 1798152 10113471 121699671 119018825 1847487 90702575 52680045 60208995 129692527 98730453 17010564 128202492 2264882 61726971 23622819 43075569 199882046 93900029 24599933 46892750 185026706 86104655 3085344 65394212 227471486 60293922 27044598 48454873 1137781 56158151 354862 135267013 103674747 38366523 18131439 1594042 16754086
1786208 1522785 60266158 125642888 228482538 98650344 74929029 2942549 2703944 13340955 6412359 18275477 1537240 154719508 120792250 77871212 115103549 104983241 140748247 105837022 145643050 1798803 10114131 121700316 119019566 1848112 90703440 52681097 60209642 129693188 98731598 17011897 128203241 2265522 61728024 23623663 43076724 199882901 93900662 24600693 46893489 185028573 86105502 3085995 65394839 227472810 60294583 27045242 48455707 1138492 56159807 357457 135268048 103675398 38367250 18132080 1594714 16754821
2,64 2,63 2,55 2,54 2,53 2,50 2,50 2,50 2,49 2,49 2,48 2,48 2,48 2,46 2,45 2,44 2,44 2,44 2,42 2,42 2,41 2,41 2,41 2,41 2,41 2,40 2,40 2,40 2,40 2,39 2,39 2,39 2,38 2,38 2,38 2,37 2,37 2,37 2,37 2,37 2,37 2,36 2,36 2,35 2,35 2,34 2,34 2,33 2,33 2,33 2,33 2,32 2,32 2,32 2,32 2,32 2,31 2,30
ARHGEF10 ASMTL PLEKHM1P SRPR GALNT2 ADAMTS17 ATP9B NAP1L4 FAM193A HS3ST3A1 MCPH1 TXNRD2 LPCAT1 INSIG1 EIF3A CD7 RNF183 MTA1 PCDHGB4 COL17A1 NFKBIL2 LETM1 DNMT1 TFCP2L1 RAB35 MAD1L1 ACTA2 KPTN GTPBP5 ST6GALNAC6 C10orf12 USP18 OPN1SW LOC284009 PRKCA NKX2-6 C5orf39 NAV1 SPTLC1 C1orf201 PRMT2 MAP6D1 LOC90784 BPHL SPRED2 RAB4A OSBPL2 MAPRE3 CCDC51 WDR37 C20orf85 AHRR REXO4 CHST11 KLF3 TBX1 WNT5B MYO10
NM_052838 NM_004574 NM_001098813 NM_001113491 NM_001154458 NM_130786 NM_033110 NM_001080438 NR_024035 NM_001086 NM_014911 NM_001088 NM_000350 NM_012089 NM_203444 NM_033151 NM_000392 NM_001023587 NM_001171 NR_003569 NR_023387 NM_007011 NM_020676 NM_007313 NM_001003408 NM_020469 NM_001092 NM_032169 NM_000017 NM_001609 NM_022735 NM_001039844 NM_020321 NM_022914 NM_000789 NM_015831 NM_147161 NM_018473 NM_006821 NM_007274 NM_005469 NM_001037171 NM_004035 NM_003501 NM_001142807 NM_001111036 NM_152282 NM_033068 NM_052957 NM_025149 NR_023316 NM_032501 NM_001141945 NM_001101 NM_005159 NM_001615 NM_016188 NM_006686
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173
Table 1 (continued ) Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr1 chr2 chr14 chr7 chr8 chr12 chr6 chr7 chr9 chr20 chr17 chr7 chr5 chr13 chr5 chr9 chr14 chr19 chr21 chr16 chr16 chr1 chr9 chr2 chr1 chr7 chr1 chr6 chr1 chrX chr7 chr20 chr3 chr10 chr3 chr9 chr10 chr22 chr16 chr6 chr17 chr5 chr2 chr7 chr1 chr19 chr5 chr1 chr17 chr19 chr7 chr17 chr1 chr10 chr10 chr7 chr10 chr1 chr5 chr12
154372213 151827549 92722258 158405247 27907931 131818564 75968244 143587044 124835446 43163505 40925157 143578873 34020027 112917772 96234968 90794507 20225056 16294245 45063979 66500283 12118128 200122439 138904005 71544899 163817579 44089644 144539510 5080145 2323386 134257081 137182964 61372176 50351011 134973176 189377910 139117469 12913471 21740231 70115140 132063624 38247695 179209213 218927406 828845 15955401 55122520 140742359 159355730 42639212 49727224 4724096 3652876 145864889 75200738 71601773 111907572 46501205 154966020 176870176 1574918
154372866 151828190 92722891 158405910 27908473 131820443 75968893 143587802 124837324 43164052 40926319 143579544 34021936 112918407 96236098 90795655 20226587 16294991 45064504 66501020 12118835 200123474 138904672 71546050 163818316 44090301 144540955 5080848 2324029 134257708 137184638 61373825 50352739 134974252 189379089 139118098 12915172 21741602 70116282 132064382 38249348 179209862 218928519 829582 15956674 55123259 140743298 159356784 42640391 49727853 4724845 3653659 145866055 75201587 71602436 111908204 46502248 154966748 176871049 1575576
2,30 2,29 2,29 2,29 2,29 2,28 2,28 2,27 2,27 2,26 2,26 2,26 2,26 2,26 2,25 2,25 2,25 2,25 2,24 2,24 2,24 2,24 2,24 2,24 2,23 2,23 2,23 2,23 2,23 2,23 2,22 2,22 2,22 2,22 2,22 2,22 2,22 2,22 2,22 2,22 2,21 2,21 2,20 2,20 2,20 2,20 2,19 2,19 2,19 2,19 2,19 2,19 2,19 2,19 2,19 2,19 2,19 2,18 2,18 2,18
LMNA RBM43 C14orf109 WDR60 SCARA5 ANKLE2 COL12A1 OR2A7 GPR21 KCNS1 PLEKHM1 OR2A20P SLC45A2 CUL4A ERAP2 C9orf47 ANG KLF2 SUMO3 PSKH1 SNX29 SHISA4 TRAF2 DYSF LOC400794 POLM GPR89A LYRM4 RER1 ZNF75D DGKI ARFGAP1 RASSF1 ZNF511 FLJ42393 MAN1B1 LOC283070 RTDR1 CHST4 OR2A4 PSME3 C5orf45 C2orf62 SUN1 FBLIM1 NUP62 PCDHGA7 NIT1 MYL4 CEACAM20 FOXK1 ITGAE GPR89B SEC24C SAR1A C7orf53 PPYR1 C1orf66 DDX41 FBXL14
NM_001102 NM_024855 NM_001616 NM_001107 NM_003474 NM_023038 NM_021794 NM_139026 NM_139055 NM_139056 NM_139057 NM_021599 NM_014694 NM_006869 NM_001025107 NM_001145407 NM_018702 NM_052853 NM_021116 NM_001116 NM_014190 NM_144650 NM_018269 NM_001127687 NM_024866 NM_001081976 NM_199162 NM_000679 NM_000684 NM_001619 NM_007002 NM_001114176 NM_001134647 NR_026892 NM_152406 NM_014423 NR_003228 NM_014914 NM_001135189 NM_018238 NM_001012727 NM_020132 NM_020133 NM_198576 NM_001138 NM_000687 NM_006621 NM_020731 NM_001624 NM_006303 NM_001042478 NM_016282 NM_003488 NM_007200 NM_001136562 NM_004857 NM_014371 NM_001145289 NM_005163 NM_001098632
174
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Table 1 (continued ) Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr11 chr2 chr20 chr18 chr1 chr8 chr5 chr2 chr10 chr4 chr9 chr3 chr17 chr5 chr5 chr22 chr1 chr11 chr7 chr21 chr4 chr14 chr2 chr17 chr1 chr2 chr17 chr3 chr22 chr19 chr13 chr1 chr10 chr7 chr12 chr16 chr14 chr21 chr9 chr11 chr13 chr20 chr16 chr20 chr1 chr1 chr1 chr1 chr15 chr9 chr11 chr7 chr5 chr5 chr19 chr15 chr7 chr15 chr19 chr4
64609997 99284710 61040935 42165845 31619982 141628099 1687959 96268657 128863488 39158359 135210801 113495155 34137596 72449727 140780698 39514927 225192145 65440964 151790200 32594464 187301973 20930859 152664922 7933308 219121014 27457537 15463136 73017682 19383009 52711228 113157300 16832002 105606512 6279408 123374687 726949 104784128 45185933 99001128 62403221 112851148 4648316 463734 48178979 43658960 90231647 9338507 201962916 61674213 135214287 116606198 23421191 180189349 140772911 46593106 32183123 134112594 84102740 2379640 8504610
64610643 99285565 61041923 42167418 31620649 141628779 1689310 96269891 128864127 39158928 135211972 113495827 34138545 72450772 140781477 39515374 225192870 65442337 151790753 32595119 187302598 20932524 152665700 7934143 219121672 27459170 15463709 73018439 19384389 52711938 113158153 16832449 105607450 6280147 123375942 727598 104785057 45186674 99001684 62404093 112851681 4649183 465061 48180250 43660815 90232482 9339158 201963647 61674782 135215030 116606846 23421918 180190218 140773568 46593861 32183750 134113325 84103387 2381804 8507474
2,18 2,17 2,17 2,17 2,17 2,17 2,17 2,17 2,17 2,17 2,16 2,16 2,16 2,16 2,16 2,15 2,15 2,15 2,15 2,15 2,15 2,14 2,14 2,14 2,14 2,14 2,14 2,13 2,13 2,13 2,13 2,13 2,13 2,13 2,13 2,13 2,12 2,12 2,12 2,12 2,12 2,12 2,12 2,12 2,12 2,12 2,11 2,11 2,11 2,11 2,11 2,11 2,11 2,11 2,10 2,10 2,10 2,10 2,10 2,10
ZFPL1 LYG1 C20orf11 RNF165 FABP3 EIF2C2 LOC728613 LOC285033 FAM196A LOC401127 SURF1 SLC9A10 MLLT6 TMEM171 PCDHGA11 SLC25A17 CABC1 C11orf68 LOC100128822 MRAP FAM149A CHD8 CACNB4 ALOX12B HLX PPM1G CDRT1 GXYLT2 TMEM191A NAPA DCUN1D2 CROCCP2 SH3PXD2A CYTH3 NCOR2 NARFL BRF1 C21orf70 ZNF322B SLC3A2 F10 PRND RAB11FIP3 TMEM189 KIAA0467 GEMIN8P4 SPSB1 ATP2B4 FBXL22 SURF2 PCSK7 IGF2BP3 LOC729678 PCDHGA10 EXOSC5 PGBD4 CALD1 KLHL25 LMNB2 C4orf23
NM_181690 NM_001012398 NM_000031 NM_001017423 NM_000693 NM_000692 NM_000691 NM_001182 NM_000034 NM_024105 NM_139178 NM_017758 NM_000697 NM_001139 NR_002710 NM_001140 NM_000698 NM_001102406 NM_020778 NM_139163 NM_006492 NM_021926 NM_001633 NM_001144 NM_030943 NM_000036 NM_000480 NM_133463 NM_001033569 NR_026903 NM_001002244 NM_013366 NM_001145 NM_015305 NM_001146 NM_001118887 NM_001142446 NM_020987 NM_016376 NM_054027 NM_015114 NM_016552 NM_017664 NM_013275 NM_152345 NR_026868 NM_001012421 NM_001012419 NM_001098805 NM_144994 NM_133475 NR_026556 NR_027020 NM_153697 NM_001115116 NM_138797 NM_024669 NM_023016 NM_001105576 NM_020140
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175
Table 1 (continued ) Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr21 chr7 chr4 chr2 chr1 chr1 chr11 chr16 chr4 chr14 chr3 chr10 chr8 chr13 chr19 chr3 chr5 chr13 chr8 chr22 chr9 chr11 chr9 chr3 chr12 chr2 chr5 chr6 chr17 chr17 chr21 chr20 chr11 chr17 chr17 chr11 chr8 chr19 chr2 chr21 chr7 chr6 chr11 chr6 chr6 chrX chr18 chr12 chr22 chr2 chr16 chr7 chr11 chr7 chr7 chr10 chr20 chr9 chr9
31952040 100322137 14984971 27657775 2429943 3546593 118708974 86505816 1374349 20525685 199363693 133647136 82769155 32487045 16001870 160000866 55068613 113213013 42413598 49319516 124682740 74136170 128925755 150533499 10972275 219816008 99751772 161502414 75803209 36558970 32671648 473097 128281912 56835395 18371849 63707734 11386701 7527601 69602478 44030904 134548861 109273995 579622 158320472 160432081 153374208 13252330 67014287 36858553 105726392 86005066 72355435 93939850 143560250 99534641 95712773 45300989 99500965 123698542
31952696 100322774 14985856 27658608 2430468 3547246 118709508 86506470 1375094 20527540 199364236 133647878 82769729 32487700 16002633 160001925 55069836 113213646 42414265 49320089 124683287 74137222 128926851 150534068 10973743 219816764 99752407 161503768 75803847 36559826 32673291 474051 128282465 56836142 18372865 63708189 11387788 7528351 69603137 44031743 134549299 109274834 580285 158322140 160434242 153374640 13253283 67014849 36859224 105727623 86005733 72356084 93940710 143560805 99535294 95713611 45301662 99501616 123699193
2,10 2,10 2,10 2,09 2,09 2,09 2,09 2,09 2,09 2,09 2,09 2,09 2,09 2,08 2,08 2,08 2,08 2,08 2,08 2,08 2,08 2,08 2,07 2,07 2,07 2,07 2,07 2,07 2,07 2,07 2,07 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,05 2,05 2,05 2,05 2,05 2,05 2,05 2,05 2,04 2,04 2,04 2,04 2,04
SOD1 SRRT C1QTNF7 C2orf16 PANK4 WDR8 RNF26 CA5A CRIPAK METT11D1 FAM157A BNIP3 SLC10A5 KL FLJ25328 MFSD1 DDX4 TMCO3 SLC20A2 ODF3B RC3H2 RNF169 RALGPS1 TM4SF18 PRR4 GLB1L LOC100133050 NCRNA00241 SGSH KRTAP4-5 URB1 CSNK2A1 KCNJ5 TBX2 FAM106A STIP1 BLK PNPLA6 AAK1 RRP1 WDR91 ARMC2 PHRF1 SYNJ2 LOC729603 SLC10A3 C18orf1 MDM1 PLA2G6 NCK2 ZCCHC14 NSUN5 PIWIL4 OR2A1 MCM7 PIPSL ZMYND8 XPA TTLL11
NM_018043 NM_006305 NM_012403 NM_012404 NR_003601 NM_174890 NM_005139 NM_001153 NM_001040084 NM_001630 NM_001637 NM_001158 NR_001557 NM_001128426 NM_012305 NM_001025205 NM_001077523 NM_006051 NM_005883 NM_153360 NM_001640 NM_080649 NM_001145646 NM_015957 NM_198544 NM_017413 NM_144772 NM_000482 NM_006789 NM_014508 NM_145298 NM_021822 NM_000483 NM_001647 NM_001638 NM_001136541 NM_030643 NM_001130415 NM_019101 NM_001136131 NM_018171 NM_175069 NM_001170 NR_026558 NM_001169 NM_173800 NM_001135190 NM_022481 NM_018209 NM_006421 NM_012402 NM_003224 NM_000045 NM_021226 NM_020876 NM_001007231 NM_199282 NM_020754 NM_025251
176
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Table 1 (continued ) Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr5 chr10 chr9 chr1 chr20 chrX chr22 chr1 chr1 chr12 chr8 chr19 chr9 chr13 chr21 chr5 chr12 chr11 chr9 chr6 chr22 chr2 chr8 chr6 chr8 chr7 chr9 chr10 chr1 chr7 chr7 chr3 chr18 chr19 chr4 chr20 chr3 chr11 chr19 chr11 chr5 chr6 chr7 chr22 chr20 chr11 chr13 chr17 chr8 chr2 chr19 chr9 chr6 chr6 chr10 chr11 chr17 chr5 chr11
153761791 111954922 35803160 64441661 43949136 48714505 18092827 109625594 68072396 112108623 144984474 45247606 37775709 23049798 45511110 140752369 48964014 116573532 126575311 18494407 19717794 190979585 23484771 1550629 146021440 72064829 129582203 74926545 226361765 98470784 100675731 129709277 69967812 2750403 7804401 51926997 197777980 66245244 2082237 71492967 114628333 90081076 149731981 37738715 37022165 57262894 113143850 4554829 103946748 70635358 16145082 115702649 33278127 44228307 35574617 130292597 36507252 111123614 124050683
153763648 111956061 35804007 64442409 43950576 48715134 18095050 109626341 68073070 112109396 144985327 45248839 37776372 23050468 45511763 140753116 48964668 116574183 126575838 18494835 19718568 190980238 23485496 1552574 146021889 72065286 129583046 74927317 226362490 98471533 100676278 129710016 69968570 2751132 7805550 51927566 197778910 66246291 2082992 71494231 114628885 90081725 149732428 37739318 37022900 57263532 113144500 4555791 103947289 70636107 16145738 115703348 33278983 44228832 35575279 130293452 36508001 111124276 124051236
2,04 2,04 2,04 2,04 2,04 2,04 2,04 2,04 2,04 2,04 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,00
GALNT10 MXI1 HINT2 UBE2U C20orf165 GRIPAP1 GP1BB PSRC1 GNG12 C12orf52 PUF60 ZNF780B EXOSC3 TNFRSF19 POFUT2 PCDHGA8 LIMA1 SIDT2 NR6A1 RNF144B SLC7A4 MFSD6 SLC25A37 FOXC1 ZNF7 NSUN5P2 SH2D3C USP54 MRPL55 SMURF1 FIS1 LOC90246 C18orf55 THOP1 AFAP1AS SUMO1P1 WDR53 SPTBN2 AP3D1 LRTOMT PGGT1B GABRR2 LOC728743 APOBEC3C DHX35 TMX2 ADPRHL1 PELP1 AZIN1 TGFA CIB3 ZNF618 SLC39A7 TMEM63B CCNY SNX19 KRTAP4-8 C5orf13 SPA17
NM_181335 NM_014629 NM_018125 NM_173728 NM_015320 NM_145735 NM_006015 NM_001040025 NM_001037164 NM_001037174 NM_015161 NM_016638 NM_032131 NM_025139 NM_016608 NM_014862 NM_001178 NM_152862 NM_032487 NM_001080523 NM_001085427 NM_000047 NM_001012301 NM_021071 NM_139058 NM_018482 NM_001135191 NM_001040445 NM_024701 NM_212556 NM_016150 NM_016116 NM_177999 NM_014034 NM_004674 NM_001672 NM_004043 NM_004192 NM_152792 NM_024083 NM_014065 NM_198186 NM_018188 NM_031921 NM_001039211 NM_033064 NM_001030287 NM_030803 NM_033388 NM_024085 NM_024490 NM_032189 NM_024524 NM_000702 NM_001135765 NM_174953 NM_001001396 NM_001002031 NM_001003713
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Table 1 (continued ) Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr4 chr14 chr2 chr10 chr1 chr10 chr7 chr1 chr17 chr1 chr4 chr1
6975976 19994926 68813855 106084059 59532773 126701787 149655954 9593002 75364548 40191655 39721670 25106856
6976625 19995487 68814386 106084715 59533669 126702422 149657392 9593729 75365507 40192402 39722341 25107403
2,00 2,00 2,00 2,00 2,00 2,00 2,00 2,00 2,00 2,00 2,00 2,00
TBC1D14 APEX1 ARHGAP25 ITPRIP FGGY CTBP2 LRRC61 TMEM201 CBX2 MFSD2A LOC344967 RUNX3
NM_001017971 NM_005765 NM_012463 NM_152565 NM_145230 NM_001695 NM_144583 NM_080653 NM_138282 NM_015941 NM_001105529 NM_138813
Table 2 Annotation of peak values indicating differentially enriched DNA methylation between the MDA-MB-231 breast cancer cells treated with resveratrol at 48 h versus non-treated cells. Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr20 chr7 chr14 chr1 chr14 chr2 chr7 chr17 chr14 chr14 chr10 chr2 chr1 chr6 chr8 chr8 chr11 chr4 chr7 chr5 chr1 chr1 chr16 chr1 chr8 chr2 chr1 chr20 chr3 chrX chr20 chr6 chr7 chr3 chr17 chrX chr14 chr19 chr1 chr11 chr13
51631293 129718140 104311019 148511761 23710633 151827549 158509814 23822375 95011537 22458926 99197678 238430809 43198303 143931574 131022998 22024534 63747908 3496220 34840781 94752293 199882134 207865542 16231473 66230912 86478784 11210550 11843395 36486806 39125418 99080841 51926997 167718803 75207943 113495155 8811092 69199270 90790629 14042256 177825607 73337521 77212180
51631942 129719263 104311666 148512420 23711373 151828190 158510485 23823405 95012580 22460289 99198211 238431646 43199496 143932238 131023436 22025287 63749057 3496869 34841438 94753044 199882991 207866280 16232198 66231596 86479521 11211221 11843983 36487535 39126567 99081873 51927566 167720348 75208630 113495728 8811749 69200037 90792432 14043117 177826556 73338348 77213337
2,33 2,33 2,32 2,31 2,31 2,30 2,27 2,26 2,24 2,24 2,24 2,20 2,20 2,19 2,17 2,17 2,16 2,16 2,15 2,15 2,14 2,14 2,14 2,13 2,13 2,13 2,12 2,12 2,12 2,12 2,11 2,11 2,10 2,10 2,10 2,10 2,09 2,09 2,09 2,08 2,08
ZNF217 CPA4 AKT1 C1orf54 REC8 RBM43 LOC154822 SLC13A2 C14orf49 PRMT5 ZDHHC16 RAMP1 SLC2A1 LOC285740 FAM49B NUDT18 TRPT1 LRPAP1 NPSR1 FAM81B NAV1 LAMB3 NOMO3 PDE4B CA1 PQLC3 NPPB SNORA71B TTC21A LOC442459 SUMO1P1 TCP10 HIP1 SLC9A10 PIK3R5 OTUD6A GPR68 LOC113230 TDRD5 DNAJB13 SLAIN1
NM_006526 NM_016352 NM_005163 NM_024579 NM_005132 NM_198557 NR_024394 NM_001145976 NM_152592 NM_006109 NM_198046 NM_005855 NM_006516 NR_027113 NM_016623 NM_024815 NM_031472 NM_002337 NM_207173 NM_152548 NM_020443 NM_001017402 NM_001004067 NM_001037341 NM_001128829 NM_152391 NM_002521 NR_002910 NM_145755 NR_024608 NR_002189 NM_004610 NM_005338 NM_183061 NM_001142633 NM_207320 NM_003485 NR_024282 NM_173533 NM_153614 NM_001040153
178
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Table 2 (continued ) Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr2 chr16 chr6 chr20 chr19 chr20 chr1 chr17 chr5 chr2 chr7 chr1 chr10 chr11 chr11 chr2 chr20 chr11 chr15 chr12 chr1 chr1 chr14 chr1
74607544 30301072 3085344 36506395 53768383 3945117 199129316 36276397 6500743 74533281 100092951 109835741 127455757 19327809 62147480 127892455 17622453 69934732 70278412 48782280 150753273 54786266 19994926 36320120
74609104 30301723 3085995 36506925 53768955 3945570 199130071 36277040 6501588 74533854 100093994 109836594 127456800 19328980 62147867 127893118 17622899 69935465 70279371 48783245 150754018 54787121 19995487 36321620
2,07 2,06 2,06 2,06 2,06 2,05 2,05 2,05 2,04 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,01 2,01 2,01 2,01 2,01 2,01 2,00 2,00
AUP1 Septin 1 BPHL SNHG11 SULT2B1 RNF24 C1orf106 KRT12 UBE2QL1 INO80B ACTL6B ATXN7L2 MMP21 NAV2 B3GAT3 PROC BANF2 CTTN PKM2 GPD1 CRCT1 ACOT11 APEX1 TEKT2
NM_181575 NM_052838 NR_026650 NR_003239 NM_177973 NM_001134338 NM_018265 NM_000223 NM_001145161 NM_031288 NM_016188 NM_153340 NM_147191 NM_001111018 NM_012200 NM_000312 NM_001159495 NM_005231 NM_182470 NM_005276 NM_019060 NM_147161 NM_080649 NM_014466
Table 3 List of hypermethylated and hypomethylated cancer genes in MDA-MB-231 cells expose to resveratrol at 24 h. Out of 2035 Hypermethylated genes, 338 were cancer-related genes:
ABCC5, ABL1, ACD, ACE, ACTB, ACTL7B, ACVR2A, ADCY1, AFF4, AJAP1, AKAP13, AKT1, ALOX12, ANGPT1, ANK3, ANKLE2, ANKRD24, APOBEC2, ARID1A, ARNT2, ASPSCR1, ATP10A, ATP2A2, ATXN3L, AXIN1, BCL2L10, BCL7A, BCOR, BMPR1A, BRD3, BTG2, C10ORF119 (MCMBP), C10ORF2, C21ORF29 (TSPEAR), C3, CACNA1D, CACNA1H, CAMTA1, CARD11, CARS, CBFA2T3, CBLB, CCDC41 (CEP83), CCDC6, CCDC81, CCNL1, CCR5, CDC25C, CDC42BPB, CDC73, CDHR2, CDHR3, CDK6, CDKN1A, CDYL, CHD3, CHD4, CIC, CNTNAP1, COL1A1, COL4A2, COL5A1, CREB3L1, CREBBP, CRLF2, CRTC1, CSDE1, CSH1, CSNK2B, CTCF, CYFIP1, CYLD, CYTSB (SPECC1), DCAF4L2, DCHS1, DCTN1, DDX41, DICER1, DIP2C, DLC1, DLEU2, DLG3, DNMT1, DNMT3A, DOCK8, DOT1L, DPP6, DRD5, DST, DYNC1I1, EGFR, EIF1AX, EIF3A, ELN, EPB41L3, EPHA1, EPHB4, ESPL1, EXOC2, EYA4, EYS, EZH2, F8, FAM123B (AMER1), FAM171A1, FAM22A (NUTM2A), FAM46C, FAT4, FBXO32, FGF19, FGFR2, FGFR3, FGFR4, FLCN, FMN2, FOXO1, FRMD7, FYN, FZD3, GATA2, GLI3, GLIPR2, GLTSCR1, GML, GNA11, GPR123, GRB2, HDAC9, HERC2, HIP1, HIST1H2AL, HIST1H3D, HLF, HOXA7, HOXD13, HPD, HSP90AA1, IDH2, IL1B, IRF2, ITGA4, JAK2, KBTBD11, KCNJ5, KDM2A, KDM2B, KDM5C, KDSR, KIAA0427 (CTIF), KIAA1024, KIAA1549, KIAA1751 (CFAP74), KIAA1804, KIF1B, KIF5B, KLF2, KLF6, KLHDC4, KLHL6, KNDC1, LDB1, LETM1, LRP2, LTK, MACF1, MAFA, MAP2K2, MAP3K1, MED1, MEN1, MLL (KMT2A), MLL3 (KMT2C), MLLT1, MLLT4, MLLT6, MMP13, MN1, MNX1, MPL, MRPS31, MSH2, MSN, MTOR, MTUS2, MYH11, MYO18B, MYO1B, MYO1G, MYO9A, MYST3 (KAT6A), NCOR2, NEURL4, NF2, NFE2L3, NIN, NLRP3, NOTCH1, NOTCH2, NOTCH3, NR4A3, NSD1, NTRK1, NUAK1, NUDT14, NUP98, ODZ2 (TENM2), OLIG2, OR2A42, OTOP1, PABPC1, PAG1, PAIP1, PAX5, PAX8, PBX1, PCSK6, PCSK7, PDCD6, PDE4DIP, PDGFB, PDGFRA, PDGFRB, PDZD2, PFKP, PHC2, PI4KA, PIK3AP1, PIK3C2B, PIK3CD, PIK3CG, PIK3R1, PKD1L2, PKP4, PLB1, PLCG1, PLXNA2, PLXNA3, PLXND1, PMS2, PNKD, PNN, POU5F1, PPARG, PPM1D, PRDM16, PRIC285 (HELZ2), PRKACA, PRKAR1A, PRKX, PTPN14, PTPRB, PTPRD, PXDN, RABEP1, RADIL, RALGDS, RBMX, RECQL4, RET, RGS12, RHOB, RHOH, RIPK1, RNF213, RNF43, RPS27, RPTOR, RUFY1, RUNDC2A (SNX29), RUNX1, RXRA, RYR2, SCN11A, SCN5A, SDHAF2, SDHB, SEPT7P2, SGK1, SH2B3, SH3GL1,
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Table 3 (continued )
Out of 1738 Hypomethylated genes, 92 were cancer-related genes:
SLC12A6, SLC9A3R1, SMARCA4, SMARCE1, SMC3, SORCS2, SOX2, SRCAP, SRSF3, SS18L1, ST6GAL2, STAT3, STC1, STK19, STYK1, SYNE2, TAF1, TAL1, TAL2, TBX18, TCHH, TERT, TFDP1, TFPT, TLL2, TLX3, TMEM132D, TMSL3 (TMSB4XP8), TNFAIP3, TNFRSF17, TNFSF8, TOP1, TP53, TPM4, TRAF7, TRAK1, TRRAP, TTC18 (CFAP70), TUBA3C, U2AF1, UBR5, VWF, WAC, WAS, WDFY3, WHSC1, WIPF2, WNT2, WT1, XBP1, XPA, XPC, ZFR2, ZFX, ZNF331, ZNF469, ZNF497, ZNF750. ABCA7, ABLIM2, AHNAK, ALS2CL, ARHGAP28, ATP2B3, ATP2C2, ATRX, C19ORF26, C1QL2, C2CD4C, CCDC63, CCND1, CCT8L2, CD79B, CDK13, CHD7, CHST1, CLK3, CNGA4, COL9A2, COX6C, CRTC3, CSMD3, CTNNA2, CYP2E1, DCAF12L2, DDB2, EGFLAM, ERCC2, ERCC6, ETV5, EVPL, FAM58A, FLI1, FLT1, FOXO3, FTCD, GNAT1, HCN1, HOXA9, IGF2, IGF2R, IKZF1, IRF4, KEAP1, KHSRP, LIFR, LMX1A, LPHN1, MED12, MSR1, MST1, MST1R, MUC6, MYCL1 (MYCL), MYD88, MYH9, MYOM2, NEUROG2, NRG2, OR51I2, P2RY8, PCDHB6, PHOX2B, PLCH2, POLE, PPP1R3A, PPP6R2, PROM1, RASGEF1A, RFTN1, RPL5, RYR1, SALL3, SEMA5B, SETBP1, SIGLEC1, SOX9, SPTBN4, STK11, TCF3, TLR2, TMPRSS2, TNFRSF14, TRAF5, TSC2, WDR24, WIF1, ZMYND10, ZNF536, ZZEF1.
Table 4 List of hypermethylated and hypomethylated genes in MDA-MB-231 cells expose to resveratrol at 48 h. Out of 1869 Hypermethylated genes, 137 were cancer-related genes:
Out of 1661 Hypomethylated genes, 288 were cancer-related genes:
ABCC5, ACSL6, AFF4, AKAP8, AKT1, ARHGAP32, ARID1B, ATP4A, BCL10, BCL11B, BPTF, BUB1B, C14ORF49 (SYNE3), CACNA1D, CALCR, CANT1, CARD10, CCDC41 (CEP83), CCNB1IP1, CDHR2, CLP1, COL1A1, CSF3R, CSH1, CSMD1, CXCR7 (ACKR3), DLG3, DNMT3A, DOCK2, DOCK8, DSE, EDNRB, EGR2, EIF1AX, EPHA1, ERG, EZH2, FAM171A1, FAM92B, FANCA, FGFR1, FMN2, G6PC, GLI3, GNA11, GNA13, GRB2, GRM8, HEATR7B2 (MROH2B), HERPUD1, HIP1, HIST1H2AL, HIST1H2BG, HIST1H4D, HOXA13, HOXD13, IRX6, ITGA4, ITGB1BP3 (NMRK2), JAK3, KALRN, KIAA1549, KIAA1804, KLHL6, LAMA4, LCK, MAFB, MAP2K3, MAP7, MCHR1, MED1, MED12L, MEF2C, MSH2, MTOR, MTUS2, MUC2, MYH11, MYO18B, MYO1B, NEK2, NEURL4, NFE2L2, NTRK1, NUAK1, NUP98, ODF4, OFD1, PABPC1, PAX8, PCDH18, PDCD6, PDHB, PIK3R5, PKD1L2, PLB1, PMS2, PNN, PNPLA7, PRF1, PROKR2, PTEN, PTPN12, RAC1, RALGDS, RET, RIPK1, RNF103, RUFY1, RUNX1, SATB2, SDHB, SDHD, SHANK1, SLC25A48, SMARCA4, SSX1, STAT6, SYK, TET3, TGFBR2, TLX3, TNFRSF17, TNFSF8, TPM3, TRAK1, TRIM33, TRPS1, TRPV6, U2AF1, U2AF2, UBE2A, UBE2D1, VANGL1, VTI1A, ZFX, ZNF765. ABCA7, ABL1, ABLIM2, ACD, AHNAK, AJAP1, ALOX12, ALS2CL, ANGPT1, ANK3, ANKLE2, ANKRD24, APOBEC2, ARHGAP28, ASPSCR1, ATP10A, ATP2A2, ATP2B3, ATP2C2, ATRX, AXIN1, BCL2L10, BCL7A, BCOR, BRD3, BTG2, C10ORF2, C19ORF26, C1QL2, C21ORF29 (TSPEAR), C2CD4C, C3, CACNA1H, CARS, CBFA2T3, CCDC6, CCDC63, CCDC81, CCND1, CCNL1, CCT8L2, CD79B, CDC42BPB, CDC73, CDK13, CDKN1A, CDYL, CHD3, CHD4, CHD7, CHST1, CLK3, CNGA4, CNTNAP1, COL4A2, COL5A1, COL9A2, COX6C, CREBBP, CRLF2, CRTC1, CRTC3, CSMD3, CSNK2B, CTNNA2, CYFIP1, CYP2E1, CYTSB (SPECC1), DCAF12L2, DCHS1, DCTN1, DDB2, DDX41, DICER1, DIP2C, DLC1, DLEU2, DNMT1, DOT1L, DPP6, DRD5, DST, EGFLAM, EGFR, EIF3A, ELN, EPHB4, ERCC2, ERCC6, ESPL1, ETV5, EVPL, EXOC2, EYS, F8, FAM22A (NUTM2A), FAM46C, FAM58A, FAT4, FGFR2, FGFR3, FGFR4, FLCN, FLI1, FLT1, FOXO1, FOXO3, FRMD7, FTCD, FYN, GATA2, GLIPR2, GML, GNAT1, GPR123, HCN1, HDAC9, HERC2, HIST1H3D, HLF, HOXA7, HOXA9, HPD, HSP90AA1, IDH2, IGF2, IGF2R, IKZF1, IL1B, IRF2, IRF4, JAK2, KCNJ5, KDM2B, KDM5C, KDSR, KEAP1, KHSRP, KIAA0427 (CTIF), KIAA1751 (CFAP74), KIF1B, KLF2, KLHDC4, KNDC1, LDB1, LETM1, LIFR, LMX1A, LPHN1, LTK, MAFA, MAP2K2, MED12, MEN1, MLL (KMT2A), MLLT1, MLLT6, MMP13, MNX1, MSN, MSR1, MST1, MST1R, MUC6, MYCL1 (MYCL), MYD88, MYH9, MYO1G, MYOM2, NCOR2, NEUROG2, NF2, NIN, NLRP3, NOTCH1, NOTCH3, NR4A3, NRG2, NSD1, NUDT14, ODZ2 (TENM2), OLIG2, OR2A42, OR51I2, P2RY8, PAG1, PAX5, PBX1, PCDHB6, PCSK6, PCSK7, PDE4DIP, PDGFRA, PDGFRB, PDZD2, PFKP, PHC2, PHOX2B, PI4KA, PIK3AP1, PIK3CG, PIK3R1, PLCG1, PLCH2, POLE, POU5F1, PPARG, PPM1D, PPP1R3A, PPP6R2, PRDM16, PRIC285 (HELZ2), PRKX, PROM1, PTPN14, PTPRB, PTPRD,
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Table 4 (continued ) PXDN, RADIL, RASGEF1A, RBMX, RFTN1, RGS12, RHOB, RHOH, RNF213, RNF43, RPL5, RPTOR, RUNDC2A (SNX29), RXRA, RYR1, SALL3, SCN11A, SCN5A, SDHAF2, SEMA5B, SEPT7P2, SETBP1, SH3GL1, SIGLEC1, SMC3, SORCS2, SOX9, SPTBN4, SRCAP, SS18L1, ST6GAL2, STC1, STK11, STK19, SYNE2, TAL2, TBX18, TCF3, TCHH, TERT, TFDP1, TFPT, TLL2, TLR2, TMEM132D, TMPRSS2, TMSL3 (TMSB4XP8), TNFRSF14, TOP1, TP53, TRAF5, TRAF7, TRRAP, TSC2, TTC18 (CFAP70), TUBA3C, WAS, WDR24, WHSC1, WIF1, WIPF2, WT1, XPA, XPC, ZFR2, ZMYND10, ZNF331, ZNF469, ZNF497, ZNF536, ZZEF1.
Table 5 Integrative analysis of DNA methylation and gene expression at 24 h of resveratrol exposure. Gene name
Fold change
Peak value
Gen expression/ Methylation status
AURKA CCNB1 DDIT4 DLGAP5 EYS FAM83D HIST1H2BK HIST1H2BM IL24 LPXN NFIL3 PFKFB3 SLC14A1 STC1 AMY1A IL18 PEG10 SLIT3 TTI1 WDR52
1,86 1,54 2,82 1,57 1,62 1,52 1,52 6,63 2,84 1,52 1,5 1,65 1,68 1,69 1,56 1,55 1,61 2,13 1,59 1,65
1,24 1,56 1,8 1,63 1,59 1,33 1,62 1,29 1,49 1,88 1,47 1,5 1,24 1,2 1,31 1,12 1,42 1,34 1,65 1,17
Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated
2. Experimental design, materials and methods 2.1. Genome-wide analysis of DNA methylation High molecular weight DNA from MDA-MB-231 triple negative breast cancer cell line untreated and treated with resveratrol (100 mM) at 24 h and 48 h was extracted using the DNeasyKit (Qiagen, Germany) according to the manufacturer's instructions. For detection of the methylation status of CpG islands (CGIs), we used array-based profiling of reference-independent methylation status (aPRIMES) technology in MDA-MB-231 cells untreated and treated with resveratrol at 24 h and 48 h. This method is based on the differential restriction and competitive hybridization of methylated and unmethylated DNA by methylation-specific and methylation-sensitive restriction enzymes, and NimbleGen HG18 Refseq Promoter 3 720 K array to measure the differential DNA methylation as described in Fig. 1. Briefly, genomic DNA (500 ng) was restricted with MseI enzyme (New England Biolabs) and ligated to adapter primers according to the recommendations of the supplier. Then, onehalf of the ligated MseI fragments were digested with the methylation-sensitive restriction enzymes HpaII and BstUI to cut unmethylated CGIs, and the remaining half is digested with the methylationspecific enzyme McrBC to cut CGIs methylated. Restricted samples were then subjected to 20 cycles of linker-mediated PCR, differentially labeled with fluorescent dyes Cy3 and Cy5, and competitively hybridized to a NimbleGen HG18 Refseq Promoter 3 720 K array following the conditions recommended by the supplier. DNA methylation analysis raw data was normalized and differential intensity
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Table 6 Integrative analysis of DNA methylation and gene expression at 48 h of resveratrol exposure. Gene name
Fold change
Peak
Gen expression/ Methylation status
GPR110 HIST1H3F HK2 MMP9 NEDD4 NFIL3 PSMD11 RUNX2 SH3KBP1 ANKRD20A3 MPHOSPH9 PEG10 SLC27A2 SLIT3 TMOD2 TTI1 XYLB
2,25 1,65 2,03 1,61 1,5 1,5 1,54 1,54 1,55 2,14 1,56 2,1 1,56 1,88 1,56 1,75 1,51
1,1063 1,5632 1,0942 1,7961 1,1856 1,3398 1,5088 1,3272 1,487 0,1 0,39 0,9 0,26 0,12 0,19 0,27 0,35
Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated
of each probe compared with experimental IP sample (IP) and control input sample (input) was calculated using the NimbleGen software DEVA. Average fold change (IP versus input) each 50 bp bin for a range of 2.44 kb upstream and 610 bp downstream window from RefSeq transcription start sites (TSS). The methylation peak values were mapped to features using DEVA software. Regions showing enrichment at 4 or more consecutive loci were integrated together to form a single “peak”. Clusters of enriched regions separated by more than 500 base pairs were integrated as separate peaks, which reflected the probability of methylation for the designated peak and/or gene at a p-value of less than 0.01. The functional annotation of target genes based on Gene Ontology was performed using DAVID (Database for Annotation, Visualization and Integrated Discovery). 2.2. Raw data processing and statistical analysis A two way ANOVA was performed to identify differentially methylated genes. Only genes with statistically significant differences in DNA methylation levels (p-value o0.05) were included.
Acknowledgements This work was supported by CONACyT SALUD (233370 and 222335). Rubiceli Medina Aguilar was supported by a CONACYT doctoral fellowship (308746).
Transparency document. Supporting information Transparency data associated with this article can be found in the online version at http://dx.doi. org/10.1016/j.dib.2017.02.006.
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DNA methylation data for identification of epigenetic targets of resveratrol in triple negative breast cancer cells Rubiceli Medina-Aguilar a, Carlos Pérez-Plasencia b, Patricio Gariglio a, Laurence A. Marchat c, Ali Flores-Pérez d, César López-Camarillo d,n, Jaime García Mena a,n a Departmento de Genética y Biología Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (Cinvestav-IPN), México City, México b Unidad de Biomedicina, FES-Iztacala UNAM, Tlalnepantla, Estado de México, México c Escuela Nacional de Medicina y Homeopatía. Red de Biotecnología. Instituto Politécnico Nacional, México City, México d Laboratorio de Oncogenómica y Proteómica del Cáncer, Universidad Autónoma de la Ciudad de México, México City, México
a r t i c l e i n f o
abstract
Article history: Received 2 November 2016 Received in revised form 6 January 2017 Accepted 2 February 2017 Available online 9 February 2017
Previous studies revealed that some bioactive food components have anti-cancer effects. However epigenetic effects of dietary compound resveratrol are largely unknown in breast cancer cells (M.A. Dawson, T. Kouzarides, 2012) [1]. Here we provide novel data and comparisons of DNA methylation status of promoter gene regions in response to resveratrol treatment at 24 h and 48 h versus untreated MDA-MB-231 breast cancer cells. DNA methylation changes were measured using Array-PRIMES method (aPRIMES) followed by whole-genome hybridization using human DNA methylation promoter microarray NimbleGen HG18 Refseq Promoter 3 720 K array. Our data were associated to corresponding changes in mRNA expression in a set of cancer-related genes. Using gene ontology analysis we also identify cancer-related cellular processes and pathways that can be epigenetically reprogramed by resveratrol. Data in this article are associated to the research articles “Methylation Landscape of Human Breast Cancer Cells in Response to Dietary Compound Resveratrol”. Medina Aguilar et al., PLoS ONE 11(6): e0157866. doi:10.1371/journal. pone.0157866 2016 (A.R. Medina, P.C. Pérez, L.A. Marchat, P.
Keywords: Breast cancer Resveratrol DNA methylation Oncogenes Tumor suppressor genes Genome-wide methylome
n
Corresponding authors. E-mail addresses: [email protected] (C. López-Camarillo), [email protected] (J. García Mena).
http://dx.doi.org/10.1016/j.dib.2017.02.006 2352-3409/& 2017 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
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Gariglio, M.J. García, C.S. Rodríguez, G.E. Ruíz, et al., 2016) [2]; and “Resveratrol inhibits cell cycle progression by targeting Aurora kinase A and Polo-like kinase 1 in breast cancer cells” in Oncology Reports. Medina Aguilar et al., 2016 Jun; 35(6):3696-704. doi: 10.3892/or.2016.4728 (A.R. Medina, P. Gariglio, M.J. García, O.E. Arechaga, S.N. Villegas, C.M. Martínez et al., 2016) [3]. & 2017 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Specifications Table Subject area More specific subject area Type of data How data was acquired Data format Experimental factors
Experimental features
Data source location Data accessibility
Biology Breast cancer, Epigenetics Tables, figure, raw data on DNA methylation (peak scores) Array-PRIMES method (aPRIMES). NimbleGen HG18 Refseq Promoter 3 720 K arrays. Filtered for peak annotation, and analyzed for differential enrichment and gene ontology DNA from untreated and treated MDA-MB-231 cells with resveratrol (100 mM) at 24 h and 48 h was extracted using the DNeasy Kit (Qiagen, Germany). To identify methylated and unmethylated DNA regions in the promoters of genes, we used Array-PRIMES method (aPRIMES). MDA-MB-231 cells were treated with resveratrol for 24 h and 48 h. For DNA methylation analysis we used NimbleGen HG18 Refseq Promoter 3 720 K array. The array covering 30,848 transcripts, 22,532 promoters, and 27,728 CpG islands. Oncogenomics and Cancer Proteomics Laboratory, UACM. México City, México. Data is available with this article.
Value of the data
First analysis on DNA methylation of promoter genes in triple negative breast cancer cells treated with resveratrol, spanning 27,728 CpG loci.
Provides genomic data indicating that resveratrol impacts the epigenetic landscape by changing DNA methylation status of specific oncogenes and tumor suppressor genes in breast cancer cells.
Analyses indicate that resveratrol epigenetically alters regulation of particular genes involved in cancer in triple negative breast cancer cells.
Data provided here serves as a novel and free resource for researchers working in the field of epigenetic regulation of cancer related genes in response to naturally occurring dietary compounds.
1. Data In this study we performed a genome-wide survey of DNA methylation in MDA-MB-231 triplenegative breast cancer cells exposed to resveratrol [1,3]. To determine the methylated and unmethylated DNA regions in the promoters of genes we used Array-PRIMES method (aPRIMES) [[4], Fig. 1]. The extensive annotation of peaks differentially enriched for DNA methylation and peak comparisons between the MDA-MB-231 breast cancer cells treated with resveratrol at 24 h and 48 h versus
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Fig. 1. Array-PRIMES procedure and NimbleGen HG18 Refseq Promoter 3 720 K arrays analysis. Genomic DNA (500 ng) was restricted to completion with MseI restriction enzyme. Then, DNA fragments produced by MseI were subjected to linkermediated PCR. Half of the resulting ligated MseI fragments were digested with McrBC restriction enzyme while the other half of MseI fragments was digested with the two methylation-sensitive endonucleases HpaII and BstUI. The experimental and control DNA was labeled with Cy3 and Cy5 nonamers. Methylated DNA fractions are highlighted in red and are expected to result in positive ratios and green spots indicate unmethylation and are to have negative ratios. DNA methylation analysis raw data was normalized and differential intensity of each probe compared with input control was calculated using the NimbleGen software DEVA. Average fold change (experimental IP sample versus Control input sample) in a range of 2.44 kb upstream and 610 bp downstream window from RefSeq transcription start sites (TSS). Modified from Pfister, S., Schlaeger, C., Mendrzyk, F., Wittmann, A., Benner, A., Kulozik, A., et al. Array-based profiling of reference-independent methylation status (aPRIMES) identifies frequent promoter methylation and consecutive downregulation of ZIC2 in pediatric medulloblastoma. Nucleic Acids Res. (2007) 35:e51.
untreated cells (Tables 1, and 2) were performed using the DEVA 1.2.1 software [2]. At 24 h treatment, 338 out of 2035 hypermethylated genes correspond to cancer genes; and 92 out of 1738 hypomethylated genes correspond to cancer genes. At 48 h treatment, 137 out of 1869 hypermethylated genes were cancer genes; and 288 out of 1661 hypomethylated genes are cancer genes (Tables 3 and 4). In addition, differentially methylated probes and differentially expressed genes were identified between the MDA-MB-231 cells treated with resveratrol at 24 h and 48 h and the MDA-MB-231 untreated. The integrative analysis of DNA methylation and gene expression at different times of resveratrol exposure showed that changes in DNA methylation were associated to corresponding changes in mRNA expression in a set of cancer-related genes (Tables 5 and 6).
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Table 1 Annotation of peak values indicating differentially enriched DNA methylation between the MDA-MB-231 breast cancer cells treated with resveratrol at 24 h versus non-treated cells. Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr8 chrX chr17 chr11 chr1 chr15 chr18 chr11 chr4 chr17 chr8 chr22 chr5 chr7 chr10 chr17 chr9 chr14 chr5 chr10 chr8 chr4 chr19 chr2 chr12 chr7 chr10 chr19 chr20 chr9 chr10 chr22 chr7 chr17 chr17 chr8 chr5 chr1 chr9 chr1 chr21 chr3 chr2 chr6 chr2 chr1 chr20 chr2 chr3 chr10 chr20 chr5 chr9 chr12 chr4 chr22 chr12 chr5
1784829 1521952 60265001 125641836 228481793 98649690 74927964 2941097 2703310 13340300 6411612 18274404 1536587 154718039 120791601 77869583 115101938 104982606 140747519 105835961 145642211 1798152 10113471 121699671 119018825 1847487 90702575 52680045 60208995 129692527 98730453 17010564 128202492 2264882 61726971 23622819 43075569 199882046 93900029 24599933 46892750 185026706 86104655 3085344 65394212 227471486 60293922 27044598 48454873 1137781 56158151 354862 135267013 103674747 38366523 18131439 1594042 16754086
1786208 1522785 60266158 125642888 228482538 98650344 74929029 2942549 2703944 13340955 6412359 18275477 1537240 154719508 120792250 77871212 115103549 104983241 140748247 105837022 145643050 1798803 10114131 121700316 119019566 1848112 90703440 52681097 60209642 129693188 98731598 17011897 128203241 2265522 61728024 23623663 43076724 199882901 93900662 24600693 46893489 185028573 86105502 3085995 65394839 227472810 60294583 27045242 48455707 1138492 56159807 357457 135268048 103675398 38367250 18132080 1594714 16754821
2,64 2,63 2,55 2,54 2,53 2,50 2,50 2,50 2,49 2,49 2,48 2,48 2,48 2,46 2,45 2,44 2,44 2,44 2,42 2,42 2,41 2,41 2,41 2,41 2,41 2,40 2,40 2,40 2,40 2,39 2,39 2,39 2,38 2,38 2,38 2,37 2,37 2,37 2,37 2,37 2,37 2,36 2,36 2,35 2,35 2,34 2,34 2,33 2,33 2,33 2,33 2,32 2,32 2,32 2,32 2,32 2,31 2,30
ARHGEF10 ASMTL PLEKHM1P SRPR GALNT2 ADAMTS17 ATP9B NAP1L4 FAM193A HS3ST3A1 MCPH1 TXNRD2 LPCAT1 INSIG1 EIF3A CD7 RNF183 MTA1 PCDHGB4 COL17A1 NFKBIL2 LETM1 DNMT1 TFCP2L1 RAB35 MAD1L1 ACTA2 KPTN GTPBP5 ST6GALNAC6 C10orf12 USP18 OPN1SW LOC284009 PRKCA NKX2-6 C5orf39 NAV1 SPTLC1 C1orf201 PRMT2 MAP6D1 LOC90784 BPHL SPRED2 RAB4A OSBPL2 MAPRE3 CCDC51 WDR37 C20orf85 AHRR REXO4 CHST11 KLF3 TBX1 WNT5B MYO10
NM_052838 NM_004574 NM_001098813 NM_001113491 NM_001154458 NM_130786 NM_033110 NM_001080438 NR_024035 NM_001086 NM_014911 NM_001088 NM_000350 NM_012089 NM_203444 NM_033151 NM_000392 NM_001023587 NM_001171 NR_003569 NR_023387 NM_007011 NM_020676 NM_007313 NM_001003408 NM_020469 NM_001092 NM_032169 NM_000017 NM_001609 NM_022735 NM_001039844 NM_020321 NM_022914 NM_000789 NM_015831 NM_147161 NM_018473 NM_006821 NM_007274 NM_005469 NM_001037171 NM_004035 NM_003501 NM_001142807 NM_001111036 NM_152282 NM_033068 NM_052957 NM_025149 NR_023316 NM_032501 NM_001141945 NM_001101 NM_005159 NM_001615 NM_016188 NM_006686
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173
Table 1 (continued ) Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr1 chr2 chr14 chr7 chr8 chr12 chr6 chr7 chr9 chr20 chr17 chr7 chr5 chr13 chr5 chr9 chr14 chr19 chr21 chr16 chr16 chr1 chr9 chr2 chr1 chr7 chr1 chr6 chr1 chrX chr7 chr20 chr3 chr10 chr3 chr9 chr10 chr22 chr16 chr6 chr17 chr5 chr2 chr7 chr1 chr19 chr5 chr1 chr17 chr19 chr7 chr17 chr1 chr10 chr10 chr7 chr10 chr1 chr5 chr12
154372213 151827549 92722258 158405247 27907931 131818564 75968244 143587044 124835446 43163505 40925157 143578873 34020027 112917772 96234968 90794507 20225056 16294245 45063979 66500283 12118128 200122439 138904005 71544899 163817579 44089644 144539510 5080145 2323386 134257081 137182964 61372176 50351011 134973176 189377910 139117469 12913471 21740231 70115140 132063624 38247695 179209213 218927406 828845 15955401 55122520 140742359 159355730 42639212 49727224 4724096 3652876 145864889 75200738 71601773 111907572 46501205 154966020 176870176 1574918
154372866 151828190 92722891 158405910 27908473 131820443 75968893 143587802 124837324 43164052 40926319 143579544 34021936 112918407 96236098 90795655 20226587 16294991 45064504 66501020 12118835 200123474 138904672 71546050 163818316 44090301 144540955 5080848 2324029 134257708 137184638 61373825 50352739 134974252 189379089 139118098 12915172 21741602 70116282 132064382 38249348 179209862 218928519 829582 15956674 55123259 140743298 159356784 42640391 49727853 4724845 3653659 145866055 75201587 71602436 111908204 46502248 154966748 176871049 1575576
2,30 2,29 2,29 2,29 2,29 2,28 2,28 2,27 2,27 2,26 2,26 2,26 2,26 2,26 2,25 2,25 2,25 2,25 2,24 2,24 2,24 2,24 2,24 2,24 2,23 2,23 2,23 2,23 2,23 2,23 2,22 2,22 2,22 2,22 2,22 2,22 2,22 2,22 2,22 2,22 2,21 2,21 2,20 2,20 2,20 2,20 2,19 2,19 2,19 2,19 2,19 2,19 2,19 2,19 2,19 2,19 2,19 2,18 2,18 2,18
LMNA RBM43 C14orf109 WDR60 SCARA5 ANKLE2 COL12A1 OR2A7 GPR21 KCNS1 PLEKHM1 OR2A20P SLC45A2 CUL4A ERAP2 C9orf47 ANG KLF2 SUMO3 PSKH1 SNX29 SHISA4 TRAF2 DYSF LOC400794 POLM GPR89A LYRM4 RER1 ZNF75D DGKI ARFGAP1 RASSF1 ZNF511 FLJ42393 MAN1B1 LOC283070 RTDR1 CHST4 OR2A4 PSME3 C5orf45 C2orf62 SUN1 FBLIM1 NUP62 PCDHGA7 NIT1 MYL4 CEACAM20 FOXK1 ITGAE GPR89B SEC24C SAR1A C7orf53 PPYR1 C1orf66 DDX41 FBXL14
NM_001102 NM_024855 NM_001616 NM_001107 NM_003474 NM_023038 NM_021794 NM_139026 NM_139055 NM_139056 NM_139057 NM_021599 NM_014694 NM_006869 NM_001025107 NM_001145407 NM_018702 NM_052853 NM_021116 NM_001116 NM_014190 NM_144650 NM_018269 NM_001127687 NM_024866 NM_001081976 NM_199162 NM_000679 NM_000684 NM_001619 NM_007002 NM_001114176 NM_001134647 NR_026892 NM_152406 NM_014423 NR_003228 NM_014914 NM_001135189 NM_018238 NM_001012727 NM_020132 NM_020133 NM_198576 NM_001138 NM_000687 NM_006621 NM_020731 NM_001624 NM_006303 NM_001042478 NM_016282 NM_003488 NM_007200 NM_001136562 NM_004857 NM_014371 NM_001145289 NM_005163 NM_001098632
174
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Table 1 (continued ) Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr11 chr2 chr20 chr18 chr1 chr8 chr5 chr2 chr10 chr4 chr9 chr3 chr17 chr5 chr5 chr22 chr1 chr11 chr7 chr21 chr4 chr14 chr2 chr17 chr1 chr2 chr17 chr3 chr22 chr19 chr13 chr1 chr10 chr7 chr12 chr16 chr14 chr21 chr9 chr11 chr13 chr20 chr16 chr20 chr1 chr1 chr1 chr1 chr15 chr9 chr11 chr7 chr5 chr5 chr19 chr15 chr7 chr15 chr19 chr4
64609997 99284710 61040935 42165845 31619982 141628099 1687959 96268657 128863488 39158359 135210801 113495155 34137596 72449727 140780698 39514927 225192145 65440964 151790200 32594464 187301973 20930859 152664922 7933308 219121014 27457537 15463136 73017682 19383009 52711228 113157300 16832002 105606512 6279408 123374687 726949 104784128 45185933 99001128 62403221 112851148 4648316 463734 48178979 43658960 90231647 9338507 201962916 61674213 135214287 116606198 23421191 180189349 140772911 46593106 32183123 134112594 84102740 2379640 8504610
64610643 99285565 61041923 42167418 31620649 141628779 1689310 96269891 128864127 39158928 135211972 113495827 34138545 72450772 140781477 39515374 225192870 65442337 151790753 32595119 187302598 20932524 152665700 7934143 219121672 27459170 15463709 73018439 19384389 52711938 113158153 16832449 105607450 6280147 123375942 727598 104785057 45186674 99001684 62404093 112851681 4649183 465061 48180250 43660815 90232482 9339158 201963647 61674782 135215030 116606846 23421918 180190218 140773568 46593861 32183750 134113325 84103387 2381804 8507474
2,18 2,17 2,17 2,17 2,17 2,17 2,17 2,17 2,17 2,17 2,16 2,16 2,16 2,16 2,16 2,15 2,15 2,15 2,15 2,15 2,15 2,14 2,14 2,14 2,14 2,14 2,14 2,13 2,13 2,13 2,13 2,13 2,13 2,13 2,13 2,13 2,12 2,12 2,12 2,12 2,12 2,12 2,12 2,12 2,12 2,12 2,11 2,11 2,11 2,11 2,11 2,11 2,11 2,11 2,10 2,10 2,10 2,10 2,10 2,10
ZFPL1 LYG1 C20orf11 RNF165 FABP3 EIF2C2 LOC728613 LOC285033 FAM196A LOC401127 SURF1 SLC9A10 MLLT6 TMEM171 PCDHGA11 SLC25A17 CABC1 C11orf68 LOC100128822 MRAP FAM149A CHD8 CACNB4 ALOX12B HLX PPM1G CDRT1 GXYLT2 TMEM191A NAPA DCUN1D2 CROCCP2 SH3PXD2A CYTH3 NCOR2 NARFL BRF1 C21orf70 ZNF322B SLC3A2 F10 PRND RAB11FIP3 TMEM189 KIAA0467 GEMIN8P4 SPSB1 ATP2B4 FBXL22 SURF2 PCSK7 IGF2BP3 LOC729678 PCDHGA10 EXOSC5 PGBD4 CALD1 KLHL25 LMNB2 C4orf23
NM_181690 NM_001012398 NM_000031 NM_001017423 NM_000693 NM_000692 NM_000691 NM_001182 NM_000034 NM_024105 NM_139178 NM_017758 NM_000697 NM_001139 NR_002710 NM_001140 NM_000698 NM_001102406 NM_020778 NM_139163 NM_006492 NM_021926 NM_001633 NM_001144 NM_030943 NM_000036 NM_000480 NM_133463 NM_001033569 NR_026903 NM_001002244 NM_013366 NM_001145 NM_015305 NM_001146 NM_001118887 NM_001142446 NM_020987 NM_016376 NM_054027 NM_015114 NM_016552 NM_017664 NM_013275 NM_152345 NR_026868 NM_001012421 NM_001012419 NM_001098805 NM_144994 NM_133475 NR_026556 NR_027020 NM_153697 NM_001115116 NM_138797 NM_024669 NM_023016 NM_001105576 NM_020140
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175
Table 1 (continued ) Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr21 chr7 chr4 chr2 chr1 chr1 chr11 chr16 chr4 chr14 chr3 chr10 chr8 chr13 chr19 chr3 chr5 chr13 chr8 chr22 chr9 chr11 chr9 chr3 chr12 chr2 chr5 chr6 chr17 chr17 chr21 chr20 chr11 chr17 chr17 chr11 chr8 chr19 chr2 chr21 chr7 chr6 chr11 chr6 chr6 chrX chr18 chr12 chr22 chr2 chr16 chr7 chr11 chr7 chr7 chr10 chr20 chr9 chr9
31952040 100322137 14984971 27657775 2429943 3546593 118708974 86505816 1374349 20525685 199363693 133647136 82769155 32487045 16001870 160000866 55068613 113213013 42413598 49319516 124682740 74136170 128925755 150533499 10972275 219816008 99751772 161502414 75803209 36558970 32671648 473097 128281912 56835395 18371849 63707734 11386701 7527601 69602478 44030904 134548861 109273995 579622 158320472 160432081 153374208 13252330 67014287 36858553 105726392 86005066 72355435 93939850 143560250 99534641 95712773 45300989 99500965 123698542
31952696 100322774 14985856 27658608 2430468 3547246 118709508 86506470 1375094 20527540 199364236 133647878 82769729 32487700 16002633 160001925 55069836 113213646 42414265 49320089 124683287 74137222 128926851 150534068 10973743 219816764 99752407 161503768 75803847 36559826 32673291 474051 128282465 56836142 18372865 63708189 11387788 7528351 69603137 44031743 134549299 109274834 580285 158322140 160434242 153374640 13253283 67014849 36859224 105727623 86005733 72356084 93940710 143560805 99535294 95713611 45301662 99501616 123699193
2,10 2,10 2,10 2,09 2,09 2,09 2,09 2,09 2,09 2,09 2,09 2,09 2,09 2,08 2,08 2,08 2,08 2,08 2,08 2,08 2,08 2,08 2,07 2,07 2,07 2,07 2,07 2,07 2,07 2,07 2,07 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,06 2,05 2,05 2,05 2,05 2,05 2,05 2,05 2,05 2,04 2,04 2,04 2,04 2,04
SOD1 SRRT C1QTNF7 C2orf16 PANK4 WDR8 RNF26 CA5A CRIPAK METT11D1 FAM157A BNIP3 SLC10A5 KL FLJ25328 MFSD1 DDX4 TMCO3 SLC20A2 ODF3B RC3H2 RNF169 RALGPS1 TM4SF18 PRR4 GLB1L LOC100133050 NCRNA00241 SGSH KRTAP4-5 URB1 CSNK2A1 KCNJ5 TBX2 FAM106A STIP1 BLK PNPLA6 AAK1 RRP1 WDR91 ARMC2 PHRF1 SYNJ2 LOC729603 SLC10A3 C18orf1 MDM1 PLA2G6 NCK2 ZCCHC14 NSUN5 PIWIL4 OR2A1 MCM7 PIPSL ZMYND8 XPA TTLL11
NM_018043 NM_006305 NM_012403 NM_012404 NR_003601 NM_174890 NM_005139 NM_001153 NM_001040084 NM_001630 NM_001637 NM_001158 NR_001557 NM_001128426 NM_012305 NM_001025205 NM_001077523 NM_006051 NM_005883 NM_153360 NM_001640 NM_080649 NM_001145646 NM_015957 NM_198544 NM_017413 NM_144772 NM_000482 NM_006789 NM_014508 NM_145298 NM_021822 NM_000483 NM_001647 NM_001638 NM_001136541 NM_030643 NM_001130415 NM_019101 NM_001136131 NM_018171 NM_175069 NM_001170 NR_026558 NM_001169 NM_173800 NM_001135190 NM_022481 NM_018209 NM_006421 NM_012402 NM_003224 NM_000045 NM_021226 NM_020876 NM_001007231 NM_199282 NM_020754 NM_025251
176
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Table 1 (continued ) Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr5 chr10 chr9 chr1 chr20 chrX chr22 chr1 chr1 chr12 chr8 chr19 chr9 chr13 chr21 chr5 chr12 chr11 chr9 chr6 chr22 chr2 chr8 chr6 chr8 chr7 chr9 chr10 chr1 chr7 chr7 chr3 chr18 chr19 chr4 chr20 chr3 chr11 chr19 chr11 chr5 chr6 chr7 chr22 chr20 chr11 chr13 chr17 chr8 chr2 chr19 chr9 chr6 chr6 chr10 chr11 chr17 chr5 chr11
153761791 111954922 35803160 64441661 43949136 48714505 18092827 109625594 68072396 112108623 144984474 45247606 37775709 23049798 45511110 140752369 48964014 116573532 126575311 18494407 19717794 190979585 23484771 1550629 146021440 72064829 129582203 74926545 226361765 98470784 100675731 129709277 69967812 2750403 7804401 51926997 197777980 66245244 2082237 71492967 114628333 90081076 149731981 37738715 37022165 57262894 113143850 4554829 103946748 70635358 16145082 115702649 33278127 44228307 35574617 130292597 36507252 111123614 124050683
153763648 111956061 35804007 64442409 43950576 48715134 18095050 109626341 68073070 112109396 144985327 45248839 37776372 23050468 45511763 140753116 48964668 116574183 126575838 18494835 19718568 190980238 23485496 1552574 146021889 72065286 129583046 74927317 226362490 98471533 100676278 129710016 69968570 2751132 7805550 51927566 197778910 66246291 2082992 71494231 114628885 90081725 149732428 37739318 37022900 57263532 113144500 4555791 103947289 70636107 16145738 115703348 33278983 44228832 35575279 130293452 36508001 111124276 124051236
2,04 2,04 2,04 2,04 2,04 2,04 2,04 2,04 2,04 2,04 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,03 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,01 2,00
GALNT10 MXI1 HINT2 UBE2U C20orf165 GRIPAP1 GP1BB PSRC1 GNG12 C12orf52 PUF60 ZNF780B EXOSC3 TNFRSF19 POFUT2 PCDHGA8 LIMA1 SIDT2 NR6A1 RNF144B SLC7A4 MFSD6 SLC25A37 FOXC1 ZNF7 NSUN5P2 SH2D3C USP54 MRPL55 SMURF1 FIS1 LOC90246 C18orf55 THOP1 AFAP1AS SUMO1P1 WDR53 SPTBN2 AP3D1 LRTOMT PGGT1B GABRR2 LOC728743 APOBEC3C DHX35 TMX2 ADPRHL1 PELP1 AZIN1 TGFA CIB3 ZNF618 SLC39A7 TMEM63B CCNY SNX19 KRTAP4-8 C5orf13 SPA17
NM_181335 NM_014629 NM_018125 NM_173728 NM_015320 NM_145735 NM_006015 NM_001040025 NM_001037164 NM_001037174 NM_015161 NM_016638 NM_032131 NM_025139 NM_016608 NM_014862 NM_001178 NM_152862 NM_032487 NM_001080523 NM_001085427 NM_000047 NM_001012301 NM_021071 NM_139058 NM_018482 NM_001135191 NM_001040445 NM_024701 NM_212556 NM_016150 NM_016116 NM_177999 NM_014034 NM_004674 NM_001672 NM_004043 NM_004192 NM_152792 NM_024083 NM_014065 NM_198186 NM_018188 NM_031921 NM_001039211 NM_033064 NM_001030287 NM_030803 NM_033388 NM_024085 NM_024490 NM_032189 NM_024524 NM_000702 NM_001135765 NM_174953 NM_001001396 NM_001002031 NM_001003713
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Table 1 (continued ) Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr4 chr14 chr2 chr10 chr1 chr10 chr7 chr1 chr17 chr1 chr4 chr1
6975976 19994926 68813855 106084059 59532773 126701787 149655954 9593002 75364548 40191655 39721670 25106856
6976625 19995487 68814386 106084715 59533669 126702422 149657392 9593729 75365507 40192402 39722341 25107403
2,00 2,00 2,00 2,00 2,00 2,00 2,00 2,00 2,00 2,00 2,00 2,00
TBC1D14 APEX1 ARHGAP25 ITPRIP FGGY CTBP2 LRRC61 TMEM201 CBX2 MFSD2A LOC344967 RUNX3
NM_001017971 NM_005765 NM_012463 NM_152565 NM_145230 NM_001695 NM_144583 NM_080653 NM_138282 NM_015941 NM_001105529 NM_138813
Table 2 Annotation of peak values indicating differentially enriched DNA methylation between the MDA-MB-231 breast cancer cells treated with resveratrol at 48 h versus non-treated cells. Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr20 chr7 chr14 chr1 chr14 chr2 chr7 chr17 chr14 chr14 chr10 chr2 chr1 chr6 chr8 chr8 chr11 chr4 chr7 chr5 chr1 chr1 chr16 chr1 chr8 chr2 chr1 chr20 chr3 chrX chr20 chr6 chr7 chr3 chr17 chrX chr14 chr19 chr1 chr11 chr13
51631293 129718140 104311019 148511761 23710633 151827549 158509814 23822375 95011537 22458926 99197678 238430809 43198303 143931574 131022998 22024534 63747908 3496220 34840781 94752293 199882134 207865542 16231473 66230912 86478784 11210550 11843395 36486806 39125418 99080841 51926997 167718803 75207943 113495155 8811092 69199270 90790629 14042256 177825607 73337521 77212180
51631942 129719263 104311666 148512420 23711373 151828190 158510485 23823405 95012580 22460289 99198211 238431646 43199496 143932238 131023436 22025287 63749057 3496869 34841438 94753044 199882991 207866280 16232198 66231596 86479521 11211221 11843983 36487535 39126567 99081873 51927566 167720348 75208630 113495728 8811749 69200037 90792432 14043117 177826556 73338348 77213337
2,33 2,33 2,32 2,31 2,31 2,30 2,27 2,26 2,24 2,24 2,24 2,20 2,20 2,19 2,17 2,17 2,16 2,16 2,15 2,15 2,14 2,14 2,14 2,13 2,13 2,13 2,12 2,12 2,12 2,12 2,11 2,11 2,10 2,10 2,10 2,10 2,09 2,09 2,09 2,08 2,08
ZNF217 CPA4 AKT1 C1orf54 REC8 RBM43 LOC154822 SLC13A2 C14orf49 PRMT5 ZDHHC16 RAMP1 SLC2A1 LOC285740 FAM49B NUDT18 TRPT1 LRPAP1 NPSR1 FAM81B NAV1 LAMB3 NOMO3 PDE4B CA1 PQLC3 NPPB SNORA71B TTC21A LOC442459 SUMO1P1 TCP10 HIP1 SLC9A10 PIK3R5 OTUD6A GPR68 LOC113230 TDRD5 DNAJB13 SLAIN1
NM_006526 NM_016352 NM_005163 NM_024579 NM_005132 NM_198557 NR_024394 NM_001145976 NM_152592 NM_006109 NM_198046 NM_005855 NM_006516 NR_027113 NM_016623 NM_024815 NM_031472 NM_002337 NM_207173 NM_152548 NM_020443 NM_001017402 NM_001004067 NM_001037341 NM_001128829 NM_152391 NM_002521 NR_002910 NM_145755 NR_024608 NR_002189 NM_004610 NM_005338 NM_183061 NM_001142633 NM_207320 NM_003485 NR_024282 NM_173533 NM_153614 NM_001040153
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Table 2 (continued ) Chromosome
Data start
Data end
Peak value ( Z 2)
Gene name
Accession number
chr2 chr16 chr6 chr20 chr19 chr20 chr1 chr17 chr5 chr2 chr7 chr1 chr10 chr11 chr11 chr2 chr20 chr11 chr15 chr12 chr1 chr1 chr14 chr1
74607544 30301072 3085344 36506395 53768383 3945117 199129316 36276397 6500743 74533281 100092951 109835741 127455757 19327809 62147480 127892455 17622453 69934732 70278412 48782280 150753273 54786266 19994926 36320120
74609104 30301723 3085995 36506925 53768955 3945570 199130071 36277040 6501588 74533854 100093994 109836594 127456800 19328980 62147867 127893118 17622899 69935465 70279371 48783245 150754018 54787121 19995487 36321620
2,07 2,06 2,06 2,06 2,06 2,05 2,05 2,05 2,04 2,02 2,02 2,02 2,02 2,02 2,02 2,02 2,01 2,01 2,01 2,01 2,01 2,01 2,00 2,00
AUP1 Septin 1 BPHL SNHG11 SULT2B1 RNF24 C1orf106 KRT12 UBE2QL1 INO80B ACTL6B ATXN7L2 MMP21 NAV2 B3GAT3 PROC BANF2 CTTN PKM2 GPD1 CRCT1 ACOT11 APEX1 TEKT2
NM_181575 NM_052838 NR_026650 NR_003239 NM_177973 NM_001134338 NM_018265 NM_000223 NM_001145161 NM_031288 NM_016188 NM_153340 NM_147191 NM_001111018 NM_012200 NM_000312 NM_001159495 NM_005231 NM_182470 NM_005276 NM_019060 NM_147161 NM_080649 NM_014466
Table 3 List of hypermethylated and hypomethylated cancer genes in MDA-MB-231 cells expose to resveratrol at 24 h. Out of 2035 Hypermethylated genes, 338 were cancer-related genes:
ABCC5, ABL1, ACD, ACE, ACTB, ACTL7B, ACVR2A, ADCY1, AFF4, AJAP1, AKAP13, AKT1, ALOX12, ANGPT1, ANK3, ANKLE2, ANKRD24, APOBEC2, ARID1A, ARNT2, ASPSCR1, ATP10A, ATP2A2, ATXN3L, AXIN1, BCL2L10, BCL7A, BCOR, BMPR1A, BRD3, BTG2, C10ORF119 (MCMBP), C10ORF2, C21ORF29 (TSPEAR), C3, CACNA1D, CACNA1H, CAMTA1, CARD11, CARS, CBFA2T3, CBLB, CCDC41 (CEP83), CCDC6, CCDC81, CCNL1, CCR5, CDC25C, CDC42BPB, CDC73, CDHR2, CDHR3, CDK6, CDKN1A, CDYL, CHD3, CHD4, CIC, CNTNAP1, COL1A1, COL4A2, COL5A1, CREB3L1, CREBBP, CRLF2, CRTC1, CSDE1, CSH1, CSNK2B, CTCF, CYFIP1, CYLD, CYTSB (SPECC1), DCAF4L2, DCHS1, DCTN1, DDX41, DICER1, DIP2C, DLC1, DLEU2, DLG3, DNMT1, DNMT3A, DOCK8, DOT1L, DPP6, DRD5, DST, DYNC1I1, EGFR, EIF1AX, EIF3A, ELN, EPB41L3, EPHA1, EPHB4, ESPL1, EXOC2, EYA4, EYS, EZH2, F8, FAM123B (AMER1), FAM171A1, FAM22A (NUTM2A), FAM46C, FAT4, FBXO32, FGF19, FGFR2, FGFR3, FGFR4, FLCN, FMN2, FOXO1, FRMD7, FYN, FZD3, GATA2, GLI3, GLIPR2, GLTSCR1, GML, GNA11, GPR123, GRB2, HDAC9, HERC2, HIP1, HIST1H2AL, HIST1H3D, HLF, HOXA7, HOXD13, HPD, HSP90AA1, IDH2, IL1B, IRF2, ITGA4, JAK2, KBTBD11, KCNJ5, KDM2A, KDM2B, KDM5C, KDSR, KIAA0427 (CTIF), KIAA1024, KIAA1549, KIAA1751 (CFAP74), KIAA1804, KIF1B, KIF5B, KLF2, KLF6, KLHDC4, KLHL6, KNDC1, LDB1, LETM1, LRP2, LTK, MACF1, MAFA, MAP2K2, MAP3K1, MED1, MEN1, MLL (KMT2A), MLL3 (KMT2C), MLLT1, MLLT4, MLLT6, MMP13, MN1, MNX1, MPL, MRPS31, MSH2, MSN, MTOR, MTUS2, MYH11, MYO18B, MYO1B, MYO1G, MYO9A, MYST3 (KAT6A), NCOR2, NEURL4, NF2, NFE2L3, NIN, NLRP3, NOTCH1, NOTCH2, NOTCH3, NR4A3, NSD1, NTRK1, NUAK1, NUDT14, NUP98, ODZ2 (TENM2), OLIG2, OR2A42, OTOP1, PABPC1, PAG1, PAIP1, PAX5, PAX8, PBX1, PCSK6, PCSK7, PDCD6, PDE4DIP, PDGFB, PDGFRA, PDGFRB, PDZD2, PFKP, PHC2, PI4KA, PIK3AP1, PIK3C2B, PIK3CD, PIK3CG, PIK3R1, PKD1L2, PKP4, PLB1, PLCG1, PLXNA2, PLXNA3, PLXND1, PMS2, PNKD, PNN, POU5F1, PPARG, PPM1D, PRDM16, PRIC285 (HELZ2), PRKACA, PRKAR1A, PRKX, PTPN14, PTPRB, PTPRD, PXDN, RABEP1, RADIL, RALGDS, RBMX, RECQL4, RET, RGS12, RHOB, RHOH, RIPK1, RNF213, RNF43, RPS27, RPTOR, RUFY1, RUNDC2A (SNX29), RUNX1, RXRA, RYR2, SCN11A, SCN5A, SDHAF2, SDHB, SEPT7P2, SGK1, SH2B3, SH3GL1,
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Table 3 (continued )
Out of 1738 Hypomethylated genes, 92 were cancer-related genes:
SLC12A6, SLC9A3R1, SMARCA4, SMARCE1, SMC3, SORCS2, SOX2, SRCAP, SRSF3, SS18L1, ST6GAL2, STAT3, STC1, STK19, STYK1, SYNE2, TAF1, TAL1, TAL2, TBX18, TCHH, TERT, TFDP1, TFPT, TLL2, TLX3, TMEM132D, TMSL3 (TMSB4XP8), TNFAIP3, TNFRSF17, TNFSF8, TOP1, TP53, TPM4, TRAF7, TRAK1, TRRAP, TTC18 (CFAP70), TUBA3C, U2AF1, UBR5, VWF, WAC, WAS, WDFY3, WHSC1, WIPF2, WNT2, WT1, XBP1, XPA, XPC, ZFR2, ZFX, ZNF331, ZNF469, ZNF497, ZNF750. ABCA7, ABLIM2, AHNAK, ALS2CL, ARHGAP28, ATP2B3, ATP2C2, ATRX, C19ORF26, C1QL2, C2CD4C, CCDC63, CCND1, CCT8L2, CD79B, CDK13, CHD7, CHST1, CLK3, CNGA4, COL9A2, COX6C, CRTC3, CSMD3, CTNNA2, CYP2E1, DCAF12L2, DDB2, EGFLAM, ERCC2, ERCC6, ETV5, EVPL, FAM58A, FLI1, FLT1, FOXO3, FTCD, GNAT1, HCN1, HOXA9, IGF2, IGF2R, IKZF1, IRF4, KEAP1, KHSRP, LIFR, LMX1A, LPHN1, MED12, MSR1, MST1, MST1R, MUC6, MYCL1 (MYCL), MYD88, MYH9, MYOM2, NEUROG2, NRG2, OR51I2, P2RY8, PCDHB6, PHOX2B, PLCH2, POLE, PPP1R3A, PPP6R2, PROM1, RASGEF1A, RFTN1, RPL5, RYR1, SALL3, SEMA5B, SETBP1, SIGLEC1, SOX9, SPTBN4, STK11, TCF3, TLR2, TMPRSS2, TNFRSF14, TRAF5, TSC2, WDR24, WIF1, ZMYND10, ZNF536, ZZEF1.
Table 4 List of hypermethylated and hypomethylated genes in MDA-MB-231 cells expose to resveratrol at 48 h. Out of 1869 Hypermethylated genes, 137 were cancer-related genes:
Out of 1661 Hypomethylated genes, 288 were cancer-related genes:
ABCC5, ACSL6, AFF4, AKAP8, AKT1, ARHGAP32, ARID1B, ATP4A, BCL10, BCL11B, BPTF, BUB1B, C14ORF49 (SYNE3), CACNA1D, CALCR, CANT1, CARD10, CCDC41 (CEP83), CCNB1IP1, CDHR2, CLP1, COL1A1, CSF3R, CSH1, CSMD1, CXCR7 (ACKR3), DLG3, DNMT3A, DOCK2, DOCK8, DSE, EDNRB, EGR2, EIF1AX, EPHA1, ERG, EZH2, FAM171A1, FAM92B, FANCA, FGFR1, FMN2, G6PC, GLI3, GNA11, GNA13, GRB2, GRM8, HEATR7B2 (MROH2B), HERPUD1, HIP1, HIST1H2AL, HIST1H2BG, HIST1H4D, HOXA13, HOXD13, IRX6, ITGA4, ITGB1BP3 (NMRK2), JAK3, KALRN, KIAA1549, KIAA1804, KLHL6, LAMA4, LCK, MAFB, MAP2K3, MAP7, MCHR1, MED1, MED12L, MEF2C, MSH2, MTOR, MTUS2, MUC2, MYH11, MYO18B, MYO1B, NEK2, NEURL4, NFE2L2, NTRK1, NUAK1, NUP98, ODF4, OFD1, PABPC1, PAX8, PCDH18, PDCD6, PDHB, PIK3R5, PKD1L2, PLB1, PMS2, PNN, PNPLA7, PRF1, PROKR2, PTEN, PTPN12, RAC1, RALGDS, RET, RIPK1, RNF103, RUFY1, RUNX1, SATB2, SDHB, SDHD, SHANK1, SLC25A48, SMARCA4, SSX1, STAT6, SYK, TET3, TGFBR2, TLX3, TNFRSF17, TNFSF8, TPM3, TRAK1, TRIM33, TRPS1, TRPV6, U2AF1, U2AF2, UBE2A, UBE2D1, VANGL1, VTI1A, ZFX, ZNF765. ABCA7, ABL1, ABLIM2, ACD, AHNAK, AJAP1, ALOX12, ALS2CL, ANGPT1, ANK3, ANKLE2, ANKRD24, APOBEC2, ARHGAP28, ASPSCR1, ATP10A, ATP2A2, ATP2B3, ATP2C2, ATRX, AXIN1, BCL2L10, BCL7A, BCOR, BRD3, BTG2, C10ORF2, C19ORF26, C1QL2, C21ORF29 (TSPEAR), C2CD4C, C3, CACNA1H, CARS, CBFA2T3, CCDC6, CCDC63, CCDC81, CCND1, CCNL1, CCT8L2, CD79B, CDC42BPB, CDC73, CDK13, CDKN1A, CDYL, CHD3, CHD4, CHD7, CHST1, CLK3, CNGA4, CNTNAP1, COL4A2, COL5A1, COL9A2, COX6C, CREBBP, CRLF2, CRTC1, CRTC3, CSMD3, CSNK2B, CTNNA2, CYFIP1, CYP2E1, CYTSB (SPECC1), DCAF12L2, DCHS1, DCTN1, DDB2, DDX41, DICER1, DIP2C, DLC1, DLEU2, DNMT1, DOT1L, DPP6, DRD5, DST, EGFLAM, EGFR, EIF3A, ELN, EPHB4, ERCC2, ERCC6, ESPL1, ETV5, EVPL, EXOC2, EYS, F8, FAM22A (NUTM2A), FAM46C, FAM58A, FAT4, FGFR2, FGFR3, FGFR4, FLCN, FLI1, FLT1, FOXO1, FOXO3, FRMD7, FTCD, FYN, GATA2, GLIPR2, GML, GNAT1, GPR123, HCN1, HDAC9, HERC2, HIST1H3D, HLF, HOXA7, HOXA9, HPD, HSP90AA1, IDH2, IGF2, IGF2R, IKZF1, IL1B, IRF2, IRF4, JAK2, KCNJ5, KDM2B, KDM5C, KDSR, KEAP1, KHSRP, KIAA0427 (CTIF), KIAA1751 (CFAP74), KIF1B, KLF2, KLHDC4, KNDC1, LDB1, LETM1, LIFR, LMX1A, LPHN1, LTK, MAFA, MAP2K2, MED12, MEN1, MLL (KMT2A), MLLT1, MLLT6, MMP13, MNX1, MSN, MSR1, MST1, MST1R, MUC6, MYCL1 (MYCL), MYD88, MYH9, MYO1G, MYOM2, NCOR2, NEUROG2, NF2, NIN, NLRP3, NOTCH1, NOTCH3, NR4A3, NRG2, NSD1, NUDT14, ODZ2 (TENM2), OLIG2, OR2A42, OR51I2, P2RY8, PAG1, PAX5, PBX1, PCDHB6, PCSK6, PCSK7, PDE4DIP, PDGFRA, PDGFRB, PDZD2, PFKP, PHC2, PHOX2B, PI4KA, PIK3AP1, PIK3CG, PIK3R1, PLCG1, PLCH2, POLE, POU5F1, PPARG, PPM1D, PPP1R3A, PPP6R2, PRDM16, PRIC285 (HELZ2), PRKX, PROM1, PTPN14, PTPRB, PTPRD,
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Table 4 (continued ) PXDN, RADIL, RASGEF1A, RBMX, RFTN1, RGS12, RHOB, RHOH, RNF213, RNF43, RPL5, RPTOR, RUNDC2A (SNX29), RXRA, RYR1, SALL3, SCN11A, SCN5A, SDHAF2, SEMA5B, SEPT7P2, SETBP1, SH3GL1, SIGLEC1, SMC3, SORCS2, SOX9, SPTBN4, SRCAP, SS18L1, ST6GAL2, STC1, STK11, STK19, SYNE2, TAL2, TBX18, TCF3, TCHH, TERT, TFDP1, TFPT, TLL2, TLR2, TMEM132D, TMPRSS2, TMSL3 (TMSB4XP8), TNFRSF14, TOP1, TP53, TRAF5, TRAF7, TRRAP, TSC2, TTC18 (CFAP70), TUBA3C, WAS, WDR24, WHSC1, WIF1, WIPF2, WT1, XPA, XPC, ZFR2, ZMYND10, ZNF331, ZNF469, ZNF497, ZNF536, ZZEF1.
Table 5 Integrative analysis of DNA methylation and gene expression at 24 h of resveratrol exposure. Gene name
Fold change
Peak value
Gen expression/ Methylation status
AURKA CCNB1 DDIT4 DLGAP5 EYS FAM83D HIST1H2BK HIST1H2BM IL24 LPXN NFIL3 PFKFB3 SLC14A1 STC1 AMY1A IL18 PEG10 SLIT3 TTI1 WDR52
1,86 1,54 2,82 1,57 1,62 1,52 1,52 6,63 2,84 1,52 1,5 1,65 1,68 1,69 1,56 1,55 1,61 2,13 1,59 1,65
1,24 1,56 1,8 1,63 1,59 1,33 1,62 1,29 1,49 1,88 1,47 1,5 1,24 1,2 1,31 1,12 1,42 1,34 1,65 1,17
Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated
2. Experimental design, materials and methods 2.1. Genome-wide analysis of DNA methylation High molecular weight DNA from MDA-MB-231 triple negative breast cancer cell line untreated and treated with resveratrol (100 mM) at 24 h and 48 h was extracted using the DNeasyKit (Qiagen, Germany) according to the manufacturer's instructions. For detection of the methylation status of CpG islands (CGIs), we used array-based profiling of reference-independent methylation status (aPRIMES) technology in MDA-MB-231 cells untreated and treated with resveratrol at 24 h and 48 h. This method is based on the differential restriction and competitive hybridization of methylated and unmethylated DNA by methylation-specific and methylation-sensitive restriction enzymes, and NimbleGen HG18 Refseq Promoter 3 720 K array to measure the differential DNA methylation as described in Fig. 1. Briefly, genomic DNA (500 ng) was restricted with MseI enzyme (New England Biolabs) and ligated to adapter primers according to the recommendations of the supplier. Then, onehalf of the ligated MseI fragments were digested with the methylation-sensitive restriction enzymes HpaII and BstUI to cut unmethylated CGIs, and the remaining half is digested with the methylationspecific enzyme McrBC to cut CGIs methylated. Restricted samples were then subjected to 20 cycles of linker-mediated PCR, differentially labeled with fluorescent dyes Cy3 and Cy5, and competitively hybridized to a NimbleGen HG18 Refseq Promoter 3 720 K array following the conditions recommended by the supplier. DNA methylation analysis raw data was normalized and differential intensity
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Table 6 Integrative analysis of DNA methylation and gene expression at 48 h of resveratrol exposure. Gene name
Fold change
Peak
Gen expression/ Methylation status
GPR110 HIST1H3F HK2 MMP9 NEDD4 NFIL3 PSMD11 RUNX2 SH3KBP1 ANKRD20A3 MPHOSPH9 PEG10 SLC27A2 SLIT3 TMOD2 TTI1 XYLB
2,25 1,65 2,03 1,61 1,5 1,5 1,54 1,54 1,55 2,14 1,56 2,1 1,56 1,88 1,56 1,75 1,51
1,1063 1,5632 1,0942 1,7961 1,1856 1,3398 1,5088 1,3272 1,487 0,1 0,39 0,9 0,26 0,12 0,19 0,27 0,35
Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated Low/hypermethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated High/hypomethylated
of each probe compared with experimental IP sample (IP) and control input sample (input) was calculated using the NimbleGen software DEVA. Average fold change (IP versus input) each 50 bp bin for a range of 2.44 kb upstream and 610 bp downstream window from RefSeq transcription start sites (TSS). The methylation peak values were mapped to features using DEVA software. Regions showing enrichment at 4 or more consecutive loci were integrated together to form a single “peak”. Clusters of enriched regions separated by more than 500 base pairs were integrated as separate peaks, which reflected the probability of methylation for the designated peak and/or gene at a p-value of less than 0.01. The functional annotation of target genes based on Gene Ontology was performed using DAVID (Database for Annotation, Visualization and Integrated Discovery). 2.2. Raw data processing and statistical analysis A two way ANOVA was performed to identify differentially methylated genes. Only genes with statistically significant differences in DNA methylation levels (p-value o0.05) were included.
Acknowledgements This work was supported by CONACyT SALUD (233370 and 222335). Rubiceli Medina Aguilar was supported by a CONACYT doctoral fellowship (308746).
Transparency document. Supporting information Transparency data associated with this article can be found in the online version at http://dx.doi. org/10.1016/j.dib.2017.02.006.
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