• Bostick, M. et al. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317, 1760–1764 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Luo, C., Hajkova, P. & Ecker, J. R. Dynamic DNA methylation: in the right place at the right time. Science 361, 1336–1340 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sato, T., Issa, J. J. & Kropf, P. DNA hypomethylating drugs in cancer therapy. Cold Spring Harb. Perspect. Med. 7, a026948 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pappalardi, M. B. et al. Discovery of a first-in-class reversible DNMT1-selective inhibitor with improved tolerability and efficacy in acute myeloid leukemia. Nat. Cancer 2, 1002–1017 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lister, R. et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462, 315–322 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jones, P. A. & Liang, G. Rethinking how DNA methylation patterns are maintained. Nat. Rev. Genet. 10, 805–811 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jeong, S. et al. Selective anchoring of DNA methyltransferases 3A and 3B to nucleosomes containing methylated DNA. Mol. Cell. Biol. 29, 5366–5376 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Weickert, P. et al. SPRTN patient variants cause global-genome DNA-protein crosslink repair defects. Nat. Commun. 14, 352 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Clements, E. G. et al. DNMT1 modulates gene expression without its catalytic activity partially through its interactions with histone-modifying enzymes. Nucleic Acids Res. 40, 4334–4346 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nabet, B. et al. Rapid and direct control of target protein levels with VHL-recruiting dTAG molecules. Nat. Commun. 11, 4687 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gruber, E., Franich, R. L., Shortt, J., Johnstone, R. W. & Kats, L. M. Distinct and overlapping mechanisms of resistance to azacytidine and guadecitabine in acute myeloid leukemia. Leukemia 34, 3388–3392 (2020).

    Article 
    PubMed 

    Google Scholar
     

  • Lin, K. H. et al. Using antagonistic pleiotropy to design a chemotherapy-induced evolutionary trap to target drug resistance in cancer. Nat. Genet. 52, 408–417 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Carnie, C. J. et al. Decitabine cytotoxicity is promoted by dCMP deaminase DCTD and mitigated by SUMO-dependent E3 ligase TOPORS. EMBO J. 43, 2397–2423 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kaito, S. et al. Inhibition of TOPORS ubiquitin ligase augments the efficacy of DNA hypomethylating agents through DNMT1 stabilization. Nat. Commun. 15, 7359 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liu, J. C. Y. et al. Concerted SUMO-targeted ubiquitin ligase activities of TOPORS and RNF4 are essential for stress management and cell proliferation. Nat. Struct. Mol. Biol. 31, 1355–1367 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Truong, P. et al. TOPORS E3 ligase mediates resistance to hypomethylating agent cytotoxicity in acute myeloid leukemia cells. Nat. Commun. 15, 7360 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tatham, M. H. et al. RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10, 538–546 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chow, K. H., Elgort, S., Dasso, M. & Ullman, K. S. Two distinct sites in Nup153 mediate interaction with the SUMO proteases SENP1 and SENP2. Nucleus 3, 349–358 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cui, Y. et al. SENP7 potentiates cGAS activation by relieving SUMO-mediated inhibition of cytosolic DNA sensing. PLoS Pathog. 13, e1006156 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kang, X. et al. SUMO-specific protease 2 is essential for suppression of polycomb group protein-mediated gene silencing during embryonic development. Mol. Cell 38, 191–201 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Langston, S. P. et al. Discovery of TAK-981, a first-in-class inhibitor of SUMO-activating enzyme for the treatment of cancer. J. Med. Chem. 64, 2501–2520 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hendriks, I. A. et al. Site-specific characterization of endogenous SUMOylation across species and organs. Nat. Commun. 9, 2456 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mehdipour, P. et al. Epigenetic therapy induces transcription of inverted SINEs and ADAR1 dependency. Nature 588, 169–173 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chiappinelli, K. B. et al. Inhibiting DNA methylation causes an interferon response in cancer via dsRNA including endogenous retroviruses. Cell 162, 974–986 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Roulois, D. et al. DNA-demethylating agents target colorectal cancer cells by inducing viral mimicry by endogenous transcripts. Cell 162, 961–973 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brocks, D. et al. DNMT and HDAC inhibitors induce cryptic transcription start sites encoded in long terminal repeats. Nat. Genet. 49, 1052–1060 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Reikine, S., Nguyen, J. B. & Modis, Y. Pattern recognition and signaling mechanisms of RIG-I and MDA5. Front. Immunol. 5, 342 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, T. et al. ADAR1 masks the cancer immunotherapeutic promise of ZBP1-driven necroptosis. Nature 606, 594–602 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chattopadhyay, S. & Sen, G. C. dsRNA-activation of TLR3 and RLR signaling: gene induction-dependent and independent effects. J. Interferon Cytokine Res. 34, 427–436 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jha, B. K. et al. Inhibition of RNase L and RNA-dependent protein kinase (PKR) by sunitinib impairs antiviral innate immunity. J. Biol. Chem. 286, 26319–26326 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Horton, J. R. et al. Structural characterization of dicyanopyridine containing DNMT1-selective, non-nucleoside inhibitors. Structure 30, 793–802 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lee, B. & Muller, M. T. SUMOylation enhances DNA methyltransferase 1 activity. Biochem. J 421, 449–461 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jones, P. A., Ohtani, H., Chakravarthy, A. & De Carvalho, D. D. Epigenetic therapy in immune-oncology. Nat. Rev. Cancer 19, 151–161 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Greenberg, M. V. C. & Bourc’his, D. The diverse roles of DNA methylation in mammalian development and disease. Nat. Rev. Mol. Cell Biol. 20, 590–607 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang, L. et al. RNF4 regulates zebrafish granulopoiesis through the DNMT1-C/EBPα axis. FASEB J. 32, 4930–4940 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hu, X. V. et al. Identification of RING finger protein 4 (RNF4) as a modulator of DNA demethylation through a functional genomics screen. Proc. Natl Acad. Sci. USA 107, 15087–15092 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Morgens, D. W. et al. Genome-scale measurement of off-target activity using Cas9 toxicity in high-throughput screens. Nat. Commun. 8, 15178 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, W. et al. MAGeCK enables robust identification of essential genes from genome-scale CRISPR/Cas9 knockout screens. Genome Biol. 15, 554 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Law, C. W., Chen, Y., Shi, W. & Smyth, G. K. voom: precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 15, R29 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Phipson, B., Lee, S., Majewski, I. J., Alexander, W. S. & Smyth, G. K. Robust hyperparameter estimation protects against hypervariable genes and improves power to detect differential expression. Ann. Appl. Stat. 10, 946–963 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wu, T. et al. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innovation (Camb.) 2, 100141 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sedlazeck, F. J., Rescheneder, P. & von Haeseler, A. NextGenMap: fast and accurate read mapping in highly polymorphic genomes. Bioinformatics 29, 2790–2791 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Neumann, T. et al. Quantification of experimentally induced nucleotide conversions in high-throughput sequencing datasets. BMC Bioinformatics 20, 258 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Picardi, E. & Pesole, G. REDItools: high-throughput RNA editing detection made easy. Bioinformatics 29, 1813–1814 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yu, Y., Ouyang, Y. & Yao, W. shinyCircos: an R/Shiny application for interactive creation of circos plot. Bioinformatics 34, 1229–1231 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Krueger, F. & Andrews, S. R. Bismark: a flexible aligner and methylation caller for bisulfite-seq applications. Bioinformatics 27, 1571–1572 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen, Y., Lun, A. T. & Smyth, G. K. From reads to genes to pathways: differential expression analysis of RNA-seq experiments using Rsubread and the edgeR quasi-likelihood pipeline. F1000Res. 5, 1438 (2016).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gu, Z., Eils, R. & Schlesner, M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32, 2847–2849 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Danecek, P. et al. Twelve years of SAMtools and BCFtools. Gigascience 10, giab008 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ritchie, M. E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Robinson, M. D. & Oshlack, A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, R25 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lund, S. P., Nettleton, D., McCarthy, D. J. & Smyth, G. K. Detecting differential expression in RNA-sequence data using quasi-likelihood with shrunken dispersion estimates. Stat. Appl. Genet. Mol. Biol. https://doi.org/10.1515/1544-6115.1826 (2012).

  • Kurtenbach, S. & Harbour, J. W. SparK: a publication-quality NGS visualization tool. Preprint at bioRxiv https://doi.org/10.1101/845529 (2019).

  • Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10–12 (2011).

    Article 

    Google Scholar
     

  • Li, Heng. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://arxiv.org/abs/1303.3997 (2013).

  • Ramirez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44, W160–W165 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, Y. et al. Model-based analysis of ChIP–seq (MACS). Genome Biol. 9, R137 (2008).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cavalcante, R. G. & Sartor, M. A. annotatr: genomic regions in context. Bioinformatics 33, 2381–2383 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mehta, S., Buyanbat, A., Orkin, S. & Nabet, B. High-efficiency knock-in of degradable tags (dTAG) at endogenous loci in cell lines. Methods Enzymol. 681, 1–22 (2023).

    CAS 
    PubMed 

    Google Scholar
     

  • Xu, Y. et al. Structural insight into SUMO chain recognition and manipulation by the ubiquitin ligase RNF4. Nat. Commun. 5, 4217 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • McCann, A. J. et al. A dominant-negative SOX18 mutant disrupts multiple regulatory layers essential to transcription factor activity. Nucleic Acids Res. 49, 10931–10955 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • McNulty, D. E. & Annan, R. S. Hydrophilic interaction chromatography reduces the complexity of the phosphoproteome and improves global phosphopeptide isolation and detection. Mol. Cell. Proteomics 7, 971–980 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kong, A. T., Leprevost, F. V., Avtonomov, D. M., Mellacheruvu, D. & Nesvizhskii, A. I. MSFragger: ultrafast and comprehensive peptide identification in mass spectrometry-based proteomics. Nat. Methods 14, 513–520 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ang, C. S. et al. Getting more out of FLAG-Tag co-immunoprecipitation mass spectrometry experiments using FAIMS. J. Proteomics 254, 104473 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367–1372 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kolbowski, L., Combe, C. & Rappsilber, J. xiSPEC: web-based visualization, analysis and sharing of proteomics data. Nucleic Acids Res. 46, W473–W478 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • MacLean, B. et al. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966–968 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pichler, A. et al. SUMO modification of the ubiquitin-conjugating enzyme E2-25K. Nat. Struct. Mol. Biol. 12, 264–269 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126–2132 (2004).

    Article 
    PubMed 

    Google Scholar
     

  • Ewels, P. A. et al. The nf-core framework for community-curated bioinformatics pipelines. Nat. Biotechnol. 38, 276–278 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Di Tommaso, P. et al. Nextflow enables reproducible computational workflows. Nat. Biotechnol. 35, 316–319 (2017).

    Article 
    PubMed 

    Google Scholar