CG methylated microarrays identify a novel methylated sequence bound by the CEBPB|ATF4 heterodimer that is active in vivo
Open accessAbstract
To evaluate the effect of CG methylation on DNA binding of sequence-specific B-ZIP transcription factors (TFs) in a high-throughput manner, we enzymatically methylated the cytosine in the CG dinucleotide on protein binding microarrays. Two Agilent DNA array designs were used. One contained 40,000 features using de Bruijn sequences where each 8-mer occurs 32 times in various positions in the DNA sequence. The second contained 180,000 features with each CG containing 8-mer occurring three times. The first design was better for identification of binding motifs, while the second was better for quantification. Using this novel technology, we show that CG methylation enhanced binding for CEBPA and CEBPB and inhibited binding for CREB, ATF4, JUN, JUND, CEBPD, and CEBPG. The CEBPB|ATF4 heterodimer bound a novel motif CGAT|GCAA 10-fold better when methylated. The electrophoretic mobility shift assay (EMSA) confirmed these results. CEBPB ChIP-seq data using primary female mouse dermal fibroblasts with 50× methylome coverage for each strand indicate that the methylated sequences well-bound on the arrays are also bound in vivo. CEBPB bound 39% of the methylated canonical 10-mers ATTGC|GCAAT in the mouse genome. After ATF4 protein induction by thapsigargin which results in ER stress, CEBPB binds methylated CGAT|GCAA in vivo, recapitulating what was observed on the arrays. This methodology can be used to identify new methylated DNA sequences preferentially bound by TFs, which may be functional in vivo.
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Among eight purified bZIP proteins, CEBPα and CEBPβ specifically bind a methylated sequence.
“Among the eight bZIP proteins, CEBPα and CEBPβ were found to specifically bind to a methylated sequence56.”
From Transcription factors as readers and effectors of DNA methylation (2016) · cites this paper as [56]
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Zhou, Q., Sun, X., Pasquier, N., Jefferson, P., Nguyen, T. T. T., Siegelin, M. D., Angelastro, J. M., & Greene, L. A. (2021) · Cancers · doi:10.3390/cancers13102504 · Cited by 37 · see citing works
“As an example, CEBPB forms functional heterodimers with ATF4, another transcription factor that protects cancer cells under stress conditions [63].”
BackgroundLi, H., Shi, L., Gao, W., Zhang, Z., Zhang, L., Zhao, Y., & Wang, G. (2022) · Methods · doi:10.1016/j.ymeth.2022.01.001 · Cited by 36 · see citing works
Bone Marrow Stroma-Induced Transcriptome and Regulome Signatures of Multiple Myeloma
Dziadowicz, S. A., Wang, L., Akhter, H., Aesoph, D., Sharma, T., Adjeroh, D., Hazlehurst, L., & Hu, G. (2022) · Cancers · doi:10.3390/cancers14040927 · Cited by 33 · see citing works
“By taking peaks not differentially accessible as the background, we identified DNA motifs corresponding to JUNB and the heterodimer of ATF::CEBP for peaks showing an increase in accessibility (Figure 6B); for completeness, we also listed the motifs for peaks showing a decrease in accessibility (Supplementary Figure S6…”
BackgroundInfluentialPredicting Preference of Transcription Factors for Methylated DNA Using Sequence Information
Liu, M., Su, W., Wang, J.-S., Yang, Y. R., Yang, H. Q., & Lin, H. (2020) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2020.07.035 · Cited by 31 · see citing works
“For example, KLF4, 6 TET, 7 CEBPA, 8 and ZFP57 9 were identi fi ed to bind to methylated DNA with high af fi nity.”
BackgroundIntegrating Epigenomics into the Understanding of Biomedical Insight
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Self-citationDetection of transcription factors binding to methylated DNA by deep recurrent neural network
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Stage 4S neuroblastoma tumors show a characteristic DNA methylation portrait
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Shared nucleotide flanks confer transcriptional competency to bZip core motifs
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Methylated Cytosines Mutate to Transcription Factor Binding Sites that Drive Tetrapod Evolution
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“Alternatively, CG dinucleotide methylation can increase DNA binding of TFs [7] resulting in repression [8] and/or activation of nearby genes [9].”
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“Genome-wide ChIP-seq and bisulfite sequencing studies for Klf4 and CEBPB show that ∼20–40% of the genomic regions bound by these proteins are methylated in vivo (50,51).”
BackgroundGrau, J., Schmidt, F., & Schulz, M. H. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad693 · Cited by 20 · see citing works
Zhan, L., Chen, M., Pang, T., Li, X., Long, L., Liang, D., Peng, L., Sun, W., & Xu, E. (2022) · Brain Pathology · doi:10.1111/bpa.13109 · Cited by 19 · see citing works
The dual role of C/EBPδ in cancer
Hartl, L., Duitman, J., Bijlsma, M. F., & Spek, C. A. (2023) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2023.103983 · Cited by 19 · see citing works
Shared Gene Targets of the ATF4 and p53 Transcriptional Networks
Baniulyte, G., Durham, S. A., Merchant, L. E., & Sammons, M. A. (2023) · Molecular and Cellular Biology · doi:10.1080/10985549.2023.2229225 · Cited by 19 · see citing works
Transcription factors read epigenetics
Hughes, T. R., & Lambert, S. A. (2017) · Science · doi:10.1126/science.aan2927 · Cited by 19 · see citing works
Self-citationGenome-wide quantification of the effects of DNA methylation on human gene regulationPreprint
Lea, A. J., Vockley, C. M., Johnston, R. A., Carpio, C. A. D., Barreiro, L. B., Reddy, T. E., & Tung, J. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/146829 · Cited by 19 · see citing works
Heyes, E. C., Wilhelmson, A. S., Wenzel, A., Manhart, G., Eder, T., Schuster, M. B., Rzepa, E., Pundhir, S., D’Altri, T., Frank, A.-K., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-41927-x · Cited by 18 · see citing works
Relevance of DNA methylation at enhancers for the acquisition of cell identities
Kreibich, E., & Krebs, A. R. (2023) · FEBS Letters · doi:10.1002/1873-3468.14686 · Cited by 18 · see citing works
Piecing together cis‐regulatory networks: insights from epigenomics studies in plants
Huang, S. C., & Ecker, J. R. (2017) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1411 · Cited by 19 · see citing works
Zhu, Y., Ye, M., Xu, H., Gu, R., Ma, X., Chen, M., Li, X., Sheng, W., & Huang, G. (2020) · Molecular Medicine Reports · doi:10.3892/mmr.2020.11535 · Cited by 18 · see citing works
“Several studies have suggested that CpG site‐specific regulation of DNA methylation could be mediated by transcription factors binding to specific gene promoter regions (51,52).”
BackgroundSyed, K. S., He, X., Tillo, D., Wang, J., Durell, S. R., & Vinson, C. (2016) · Biochemistry · doi:10.1021/acs.biochem.6b00796 · Cited by 18 · see citing works
Self-citationXu, X., Zhang, Y., Pan, Z., Zhang, X., Liu, X., Tang, L., Zhang, X., Zhou, F., & Cheng, H. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1057839 · Cited by 17 · see citing works
“Accordingly, the most prominent motifs enriched at DNA hypermethylation sites in psoriatic Munro’s microabscess, favoring the promotion of the recruitment of neutrophils predominantly, can be bound by AP1-family TFs.”
BackgroundInfluentialKranzhöfer, D. K., Gilsbach, R., Grüning, B., Backofen, R., Nührenberg, T., & Hein, L. (2016) · PLoS ONE · doi:10.1371/journal.pone.0166575 · Cited by 21 · see citing works
Finding de novo methylated DNA motifs
Ngo, V., Wang, M., & Wang, W. T. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz079 · Cited by 14 · see citing works
Pioneer factors and their in vitro identification methods
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“DNA methylation inhibits JunD binding [71, 72], thereby potentially providing a causal mechanism for the regulation of gene expression by methylation at these sites.”
BackgroundNikolova, E. N., Stanfield, R. L., Dyson, H. J., & Wright, P. E. (2020) · Biochemistry · doi:10.1021/acs.biochem.0c00253 · Cited by 14 · see citing works
Arai, N., Ohno, Y., Jumyo, S., Hamaji, Y., & Ohyama, T. (2020) · Journal of Experimental Botany · doi:10.1093/jxb/eraa560 · Cited by 13 · see citing works
“A transcription factorimplicated mechanism is also possible, as some transcription factors cannot bind to their target sequences when they are methylated, thus preventing transcription initiation (Mann et al., 2013; O’Malley et al., 2016; Yin et al., 2017).”
BackgroundDeciphering the dynamic code: DNA recognition by transcription factors in the ever-changing genome
Yao, Y. M., Miodownik, I., O’Hagan, M., Jbara, M., & Afek, A. (2024) · Transcription · doi:10.1080/21541264.2024.2379161 · Cited by 12 · see citing works
“These methods, such as methylated protein-binding microarrays [60], methyl-spec-seq [61], bisulfite-SELEX [62], epi-SELEX [63], methyl-DNAshape [64] and others, have facilitated the determination of binding preferences of hundreds of TFs to sites containing methylated CpG, greatly increasing our…”
Identifying the “stripe” transcription factors and cooperative binding related to DNA methylation
Luo, X., & Zou, Q. (2024) · Communications Biology · doi:10.1038/s42003-024-06992-y · Cited by 11 · see citing works
Ao, X., Sa, R., Wang, J., Dao, R., Wang, H., & Yu, H. (2016) · Cytotechnology · doi:10.1007/s10616-016-9988-8 · Cited by 11 · see citing works
“A mass spectrometry-based screen and a protein-binding microarray approach were recently used to identify transcription factors that preferentially bind to methylated CpG sites (Hu et al. 2013; Mann et al. 2013).”
BackgroundChatterjee, R., He, X., Huang, D., FitzGerald, P. C., Smith, A. D., & Vinson, C. (2014) · Epigenetics & Chromatin · doi:10.1186/1756-8935-7-35 · Cited by 11 · see citing works
“We compared the fibroblast [31] and keratinocyte HMRs to identify overlapping and tissue-specific HMRs.”
InfluentialSelf-citationRay, S., Tillo, D., Assad, N., Ufot, A., Deppmann, C. D., Durell, S. R., Porollo, A., & Vinson, C. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.05.080 · Cited by 10 · see citing works
Self-citationCui, T., Huang, J., Sun, Y., Ning, B., Mu, F., You, X., Guo, Y., Li, H., & Wang, N. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.627102 · Cited by 9 · see citing works
“For example, KLFs 4, 5, 6, 9, and 15 have been shown to promote preadipocyte differentiation (Dan et al., 2005; Enomoto et al., 2013; Mann et al., 2013; Soroush et al., 2013; Kimura and Fujimori, 2014; Escalona-Nandez et al., 2015), whereas KLFs 2, 3, 7, 10, and 16 inhibit preadipocyte…”
BackgroundLoureiro, C. M., Fachim, H., Zuelli, F. M. D. G. C., Shuhama, R., Menezes, P. R., Dalton, C., Del‐Ben, C. M., Reynolds, G. P., & Louzada‐Júnior, P. (2021) · Epigenomics · doi:10.2217/epi-2020-0451 · Cited by 9 · see citing works
Hernández-Corchado, A., & Najafabadi, H. S. (2022) · Genome biology · doi:10.1186/s13059-022-02713-y · Cited by 7 · see citing works
“The JAMS model for CEBPB (Fig.”
BackgroundInfluentialEpigenetic features in regulation of telomeres and telomerase in stem cells
Doğan, F., & Forsyth, N. R. (2021) · Emerging Topics in Life Sciences · doi:10.1042/etls20200344 · Cited by 8 · see citing works
Reading cytosine modifications within chromatin
Mahé, E. A., Madigou, T., & Salbert, G. (2018) · Transcription · doi:10.1080/21541264.2017.1406435 · Cited by 9 · see citing works
“MAX bHLH CACGTG Gel-shift C, 5caC [48] MAX bHLH TGACGCGCGCG Pull-down, MS/MS C [22] MAX bHLH CACGTG SELEX C [27] Tcf3/Ascl1 bHLH CGCAGGTG Gel-shift 5caC [49] Tcf4 bHLH ACACGTG DNA array 5hmC [50] USF-1 bHLH ACACGTG DNA array C [50] ARNT2 bHLH AAACGCTTCC Protein microarray 5mC [25] CREB1 bZIP TGACGTCA DNA array C [28]…”
TET2 binding to enhancers facilitates transcription factor recruitment in hematopoietic cellsPreprint
Rasmussen, K. D., Berest, I., Kessler, S., Nishimura, K., Simón-Carrasco, L., Vassilou, G. S., Pedersen, M. T., Christensen, J. F., Zaugg, J. B., & Helin, K. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/336008 · Cited by 9 · see citing works
Santarelli, R., Pascucci, G. R., Presti, S. L., Crosta, M. D., Benedetti, R., Neri, A., Gonnella, R., & Cirone, M. (2024) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2024.195064 · Cited by 7 · see citing works
Ray, S., Tillo, D., Assad, N., Ufot, A., Porollo, A. A., Durell, S., & Vinson, C. (2021) · ACS Omega · doi:10.1021/acsomega.1c04148 · Cited by 5 · see citing works
Self-citationNishizaki, S. S., & Boyle, A. P. (2022) · BMC Bioinformatics · doi:10.1186/s12859-022-04865-x · Cited by 7 · see citing works
“CEBPB has been reported to preferentially bind to methylated sequence, thus the discrepancy in predictions has previously been thought to be a result of limited genome methylated sequence availability, a necessity for calculating more accurate predictions in SEMplMe (Mann et al., 2013).”
MethodResultInfluentialLocus- and cell type-specific epigenetic switching during cellular differentiation in mammals
Zhao, Y.-T., Fasolino, M., & Zhou, Z. (2016) · Frontiers in Biology · doi:10.1007/s11515-016-1411-5 · Cited by 8 · see citing works
Bie, L., Du, L., Yuan, Q., & Gao, J. (2018) · Journal of Molecular Modeling · doi:10.1007/s00894-018-3678-8 · Cited by 7 · see citing works
Rovirosa, L., Ramos-Morales, A., & Javierre, B. M. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.592087 · Cited by 5 · see citing works
DNA methylation shapes transcription factor binding beyond canonical CpG contexts
Miodownik, I., Solozabal, R., O’Hagan, M., Albeck, S., Peleg, Y., Takáč, M., & Afek, A. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2520814122 · Cited by 6 · see citing works
Using methylation data to improve transcription factor binding prediction
Morgan, D. C., DeMeo, D. L., & Glass, K. (2024) · Epigenetics · doi:10.1080/15592294.2024.2309826 · Cited by 6 · see citing works
“CEBPβ has previously been found to bind nearly equally well to both methylated and unmethylated versions of its binding site [34], and both CEBPα and CEBPβ have been shown to bind to a methylated version of the consensus CREB binding site [33], indicating that methylation levels may have only…”
Höglund, A., Henriksen, R., Churcher, A. M., Guerrero‐Bosagna, C., Barrio, Á. M., Johnsson, M., Jensen, P., & Wright, D. (2024) · PLoS Genetics · doi:10.1371/journal.pgen.1010719 · Cited by 6 · see citing works
Molecular Signatures of CB-6644 Inhibition of the RUVBL1/2 Complex in Multiple Myeloma
Yi, W., Dziadowicz, S. A., Mangano, R. S., Wang, L., McBee, J. C., Frisch, S. M., Hazlehurst, L., Adjeroh, D., & Hu, G. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25169022 · Cited by 6 · see citing works
“Both ATF4::CEBP and IRF4 are implicated as pioneer transcription factors promoting chromatin accessibility at their target sites [59–64].”
BackgroundArdıçlı, S., Yigitgor, P., Babayev, H., Özen, D., Bozkurt, B., Şentürk, N., Pilli, M., SALCI, H., & Intas, D. S. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e37716 · Cited by 6 · see citing works
“CpG methylation directly represses transcription by preventing the binding of some transcription factors (TFs) to their recognition motifs [64,65].”
BackgroundVidarsdóttir, L., Fernandes, R. V., Zachariadis, V., Das, I., Edsbäcker, E., Sigvaldadóttir, I., Azimi, A., Höiom, V., Hansson, J., Grandér, D., et al. (2020) · Melanoma Research · doi:10.1097/cmr.0000000000000675 · Cited by 6 · see citing works
Hydroxycarbamide effects on DNA methylation and gene expression in myeloproliferative neoplasmsPreprint
Castillo, S. C., Montibus, B., Rocha, A. V., Duke, W., von Meyenn, F., McLornan, D. P., Harrison, C. N., Mullally, A., Schulz, R., & Oakey, R. J. (2021) · Genome Research · doi:10.1101/gr.270066.120 · Cited by 6 · see citing works
Methylome of human senescent hematopoietic progenitors
Capone, S., Colombo, A., Johnson, B. K., Triche, T. J., & Ramsingh, G. (2018) · Experimental Hematology and Oncology · doi:10.1186/s40164-018-0123-8 · Cited by 5 · see citing works
GPS2 confers l -asparaginase resistance in acute lymphoblastic leukemia cells through ATF4/ASNS axis
Chen, J., Luo, J., Liu, Y., Zhou, J., Cui, H., & Deng, L. (2025) · Carcinogenesis · doi:10.1093/carcin/bgaf035 · Cited by 4 · see citing works
Thompson, D., Odufuwa, A. E., Brissette, C. A., & Watt, J. A. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1223273 · Cited by 4 · see citing works
“Furthermore, several studies have shown that AP-1 binding is inhibited by hypermethylation at or near to their binding motif (Mann et al., 2013; Yin et al., 2017; Héberlé and Bardet, 2019).”
BackgroundGABPα Binding to Overlapping ETS and CRE DNA Motifs Is Enhanced by CREB1: Custom DNA Microarrays
He, X., Syed, K. S., Tillo, D., Mann, I. K., Weirauch, M. T., & Vinson, C. (2015) · G3 Genes Genomes Genetics · doi:10.1534/g3.115.020248 · Cited by 4 · see citing works
“…DNA binding preferences of TFs. Recently, we and others have used PBMs with custom-designed probe sequences to interrogate the binding speci fi cities of heterodimeric interactions between members of the same TF family (Bolotin et al. 2010; Siggers et al. 2012; Mann et al. 2013; Gordan et al. 2013).”
Self-citationDatabases and prospects of dynamic gene regulation in eukaryotes: A mini review
Chow, C.-N., Yang, C.-W., & Chang, W. (2023) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2023.03.032 · Cited by 5 · see citing works
The bZIP mutant CEBPB (V285A) has sequence specific DNA binding propensities similar to CREB1
Ray, S., Ufot, A., Assad, N., Singh, J., Durell, S. R., Porollo, A., Tillo, D., & Vinson, C. (2019) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2019.02.002 · Cited by 4 · see citing works
“To examine the effect of this amino acid position on the recognition of methylated DNA, we generated reciprocal mutants creating CEBPΒ(V285A) and CREB1(A297V) and examined binding to four types of double-stranded DNA (dsDNA) containing modified cytosines (5mC and it’s oxidative product 5‐hydroxymethylcytosine, or 5hmC…”
BackgroundMethodResultInfluentialSelf-citationGrau, J., Schmidt, F., & Schulz, M. H. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.21.348193 · Cited by 4 · see citing works
“Specifically, CEBPB ( 25 , 61 , 62 ), SMAD5 ( 23 ) and ZBTB33 ( 23 , 72 , 73 ) have been reported to prefer methylated DNA, but we did not observe a significant and consistent improvement of prediction performance in our study.”
ResultNerlich, A. G., Janze, N., & Goethe, R. (2021) · Genes and Immunity · doi:10.1038/s41435-021-00153-5 · Cited by 3 · see citing works
Ray, S., Tillo, D., Ufot, A., Assad, N., Durell, S. R., & Vinson, C. (2020) · Biochemistry · doi:10.1021/acs.biochem.0c00475 · Cited by 3 · see citing works
Self-citation
- Authors
- Mann, I. K., Chatterjee, R., Zhao, J., He, X., Weirauch, M. T., Hughes, T. R., & Vinson, C.
- Affiliations
- National Institutes of Health (US)
- Cincinnati Children's Hospital Medical Center (US)
- University of Toronto (CA)
- Corresponding author
- Hughes, Timothy R.
- Vinson, Charles
- ORCID
- Venue
- Genome Research
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2013-04-16
- Volume
- 23
- Issue
- 6
- Pages
- 988-997
- ISSN
- 1088-9051 (ISSN-L)
- PMC
- PMC3668366
- OpenAlex
- W2078641190
- Cited by
- 126
- References
- 50
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 13 · 2023: 9 · 2022: 14 · 2021: 11 · 2020: 12 · 2019: 10 · 2018: 10 · 2017: 13 · 2016: 10 · 2015: 7 · 2014: 4 · 2013: 2
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genome Research (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- National Institutes of Health
- National Cancer Institute
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cancer-related gene regulation
- Keywords
- DNA methylation, CEBPB, ATF4, protein-DNA interactions, CEBPA, CREB, c-Jun, endoplasmic reticulum stress, thapsigargin, methylome
- MeSH terms
- Animals, Base Sequence, Binding Sites, Female, Fibroblasts, Protein Binding, Transcription Factors, CpG Islands, DNA Methylation, Thapsigargin, CCAAT-Enhancer-Binding Protein-beta, Mice, Activating Transcription Factor 4, Protein Multimerization, Position-Specific Scoring Matrices, Nucleotide Motifs
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