A modular dCas9-SunTag DNMT3A epigenome editing system overcomes pervasive off-target activity of direct fusion dCas9-DNMT3A constructs
Open accessPublished version of a preprint
Abstract
Detection of DNA methylation in the genome has been possible for decades; however, the ability to deliberately and specifically manipulate local DNA methylation states in the genome has been extremely limited. Consequently, this has impeded our understanding of the direct effect of DNA methylation on transcriptional regulation and transcription factor binding in the native chromatin context. Thus, highly specific targeted epigenome editing tools are needed to address this. Recent adaptations of genome editing technologies, including fusion of the DNMT3A DNA methyltransferase catalytic domain to catalytically inactive Cas9 (dC9-D3A), have aimed to alter DNA methylation at desired loci. Here, we show that these tools exhibit consistent off-target DNA methylation deposition in the genome, limiting their capabilities to unambiguously assess the functional consequences of DNA methylation. To address this, we developed a modular dCas9-SunTag (dC9Sun-D3A) system that can recruit multiple DNMT3A catalytic domains to a target site for editing DNA methylation. dC9Sun-D3A is tunable, specific, and exhibits much higher induction of DNA methylation at target sites than the dC9-D3A direct fusion protein. Importantly, genome-wide characterization of dC9Sun-D3A binding sites and DNA methylation revealed minimal off-target protein binding and induction of DNA methylation with dC9Sun-D3A, compared to pervasive off-target methylation by dC9-D3A. Furthermore, we used dC9Sun-D3A to demonstrate the binding sensitivity to DNA methylation for CTCF and NRF1 in situ. Overall, this modular dC9Sun-D3A system enables precise DNA methylation deposition with the lowest off-target DNA methylation levels reported to date, allowing accurate functional determination of the role of DNA methylation at single loci.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Local amplification of regulator concentration through protein or RNA scaffolding has been incorporated into epigenetic editing to enhance the on-target to off-target ratio.
“Local amplification of regulator concentration through protein (SunTag) or RNA scaffolding (e.g. Casilio) has been incorporated into epigenetic editing to enhance the on/off target ratio (Fig. 3).”
From Dynamic DNA methylation: In the right place at the right time (2018) · cites this paper as [58]
Scaffolding allows multiple copies of epigenetic effectors to be tethered to a genomic site, providing more robust on-target modulation and reduced non-specific effects.
“This scaffold allows multiple copies of epigenetic effectors (e.g. DNMT3A catalytic domain) to be tethered to a genomic site, providing more robust on-target modulation and reduced non-specific effects (58).”
From Dynamic DNA methylation: In the right place at the right time (2018) · cites this paper as [58]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Trimmomatic: a flexible trimmer for Illumina sequence data
Bolger, A. M., Lohse, M., & Usadel, B. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu170 · Cited by 65,548 · see citing works
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849 · see citing works
Enzymatic assembly of DNA molecules up to several hundred kilobases
Gibson, D. G., Young, L., Chuang, R.-Y., Venter, J. C., Hutchison, C. A., & Smith, H. O. (2009) · Nature Methods · doi:10.1038/nmeth.1318 · Cited by 9,742 · see citing works
RNA-Guided Human Genome Engineering via Cas9
Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., DiCarlo, J. E., Norville, J. E., & Church, G. M. (2013) · Science · doi:10.1126/science.1232033 · Cited by 9,210 · see citing works
Okano, M., Bell, D. W., Haber, D. A., & Li, E. (1999) · Cell · doi:10.1016/s0092-8674(00)81656-6 · Cited by 6,143 · see citing works
Repurposing CRISPR as an RNA-Guided Platform for Sequence-Specific Control of Gene Expression
Qi, L. S., Larson, M. H., Gilbert, L. A., Doudna, J. A., Weissman, J. S., Arkin, A. P., & Lim, W. A. (2013) · Cell · doi:10.1016/j.cell.2013.02.022 · Cited by 5,016 · cited 2× · see citing works
“The direct fusion of dCas9 to the catalytic domain of DNMT3Awas previously reported and used to induce cytosine methylation at targeted loci (Qi et al. 2013; Amabile et al. 2016; Liu et al. 2016; Vojta et al. 2016; Stepper et al. 2017).”
BackgroundHuman DNA methylomes at base resolution show widespread epigenomic differences
Lister, R., Pelizzola, M., Dowen, R. H., Hawkins, R. D., Hon, G., Tonti-Filippini, J., Nery, J. R., Lee, L., Ye, Z., Ngo, Q.-M., et al. (2009) · Nature · doi:10.1038/nature08514 · Cited by 4,673 · see citing works
Self-citationTargeted mutation of the DNA methyltransferase gene results in embryonic lethality
Li, E., Bestor, T. H., & Jaenisch, R. (1992) · Cell · doi:10.1016/0092-8674(92)90611-f · Cited by 3,984 · see citing works
Epigenetics in human disease and prospects for epigenetic therapy
Egger, G., Liang, G., Aparicio, A., & Jones, P. A. (2004) · Nature · doi:10.1038/nature02625 · Cited by 3,232 · see citing works
DNA methylation: roles in mammalian development
Smith, Z. D., & Meissner, A. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3354 · Cited by 3,045 · see citing works
MethPrimer: designing primers for methylation PCRs
Li, L.-C., & Dahiya, R. (2002) · Bioinformatics · doi:10.1093/bioinformatics/18.11.1427 · Cited by 2,741 · see citing works
Sambamba: fast processing of NGS alignment formats
Tarasov, A., Vilella, A. J., Cuppen, E. P. J. G., Nijman, I. J., & Prins, P. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv098 · Cited by 2,339 · see citing works
Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning
Cokus, S. J., Feng, S.-H., Zhang, X.-Y., Chen, Z., Merriman, B., Haudenschild, C., Pradhan, S., Nelson, S., Pellegrini, M., & Jacobsen, S. (2008) · Nature · doi:10.1038/nature06745 · Cited by 2,278 · see citing works
Irizarry, R. A., Ladd-Acosta, C., Wen, B., Wu, Z., Montano, C., Onyango, P., Cui, H., Gabo, K., Rongione, M., Webster, M., et al. (2009) · Nature Genetics · doi:10.1038/ng.298 · Cited by 2,177 · see citing works
Bernstein, B. E., Meissner, A., & Lander, E. S. (2007) · Cell · doi:10.1016/j.cell.2007.01.033 · Cited by 2,086 · see citing works
Global epigenomic reconfiguration during mammalian brain development
Lister, R., Mukamel, E. A., Nery, J. R., Urich, M., Puddifoot, C. A., Johnson, N. D., Lucero, J., Huang, Y., Dwork, A. J., Schultz, M. D., et al. (2013) · Science · doi:10.1126/science.1237905 · Cited by 1,830 · see citing works
Self-citationConserved role of intragenic DNA methylation in regulating alternative promoters
Maunakea, A. K., Nagarajan, R. P., Bilenky, M., Ballinger, T. J., D’Souza, C., Fouse, S. D., Johnson, B. E., Hong, C., Nielsen, C., Zhao, Y., et al. (2010) · Nature · doi:10.1038/nature09165 · Cited by 1,743 · see citing works
A Protein-Tagging System for Signal Amplification in Gene Expression and Fluorescence Imaging
Tanenbaum, M. E., Gilbert, L. A., Qi, L. S., Weissman, J. S., & Vale, R. D. (2014) · Cell · doi:10.1016/j.cell.2014.09.039 · Cited by 1,560 · see citing works
CTCF: Master Weaver of the Genome
Phillips‐Cremins, J. E., & Corces, V. G. (2009) · Cell · doi:10.1016/j.cell.2009.06.001 · Cited by 1,540 · see citing works
DNA-binding factors shape the mouse methylome at distal regulatory regions
Stadler, M. B., Murr, R., Burger, L., Ivanek, R., Lienert, F., Schöler, A., Nimwegen, E. V., Wirbelauer, C., Oakeley, E. J., Gaidatzis, D., et al. (2011) · Nature · doi:10.1038/nature10716 · Cited by 1,383 · see citing works
Kim, J. H., Lee, S. R., Li, L.-H., Park, H., Park, J.-H., Lee, K. Y., Kim, M., Shin, B. A., & Choi, S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018556 · Cited by 1,340 · see citing works
CRISPRscan: designing highly efficient sgRNAs for CRISPR-Cas9 targeting in vivo
Moreno-Mateos, M. A., Vejnar, C. E., Beaudoin, J.-D., Fernandez, J. P., Mis, E. K., Khokha, M. K., & Giraldez, A. J. (2015) · Nature Methods · doi:10.1038/nmeth.3543 · Cited by 1,290 · see citing works
Impact of cytosine methylation on DNA binding specificities of human transcription factors
Yin, Y., Morgunova, E., Jolma, A., Kaasinen, E., Sahu, B., Khund-Sayeed, S., Das, P. K., Kivioja, T., Dave, K., Zhong, F., et al. (2017) · Science · doi:10.1126/science.aaj2239 · Cited by 1,257 · see citing works
Editing DNA Methylation in the Mammalian Genome
Liu, X. S., Wu, H., Ji, X., Stelzer, Y., Wu, X., Czauderna, S., Shu, J., Dadon, D., Young, R. A., & Jaenisch, R. (2016) · Cell · doi:10.1016/j.cell.2016.08.056 · Cited by 1,224 · cited 7× · see citing works
“Previous work has highlighted the ability of dCas9 to be used to induce DNA methylation at desired regions in the genome(Vojta et al. 2016; Amabile et al. 2016; Liu et al. 2016; Lei et al. 2017; Stepper et al. 2017).”
BackgroundMethodInfluentialGNU Parallel: The Command-Line Power Tool.
Tange, O. (2011) · Cited by 934 · see citing works
Repurposing the CRISPR-Cas9 system for targeted DNA methylation
Vojta, A., Dobrinić, P., Tadić, V., Bočkor, L., Korać, P., Jülg, B. D., Klasić, M., & Zoldoš, V. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw159 · Cited by 772 · see citing works
Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation
Jackson-Grusby, L., Beard, C., Possemato, R., Tudor, M., Fambrough, D., Csankovszki, G., Dausman, J., Lee, P., Wilson, C., Lander, E., et al. (2001) · Nature Genetics · doi:10.1038/83730 · Cited by 694 · see citing works
A transcription activator-like effector toolbox for genome engineering
Sanjana, N. E., Cong, L., Zhou, Y., Cunniff, M. M., Feng, G., & Zhang, F. (2012) · Nature Protocols · doi:10.1038/nprot.2011.431 · Cited by 628 · see citing works
Widespread plasticity in CTCF occupancy linked to DNA methylation
Wang, H., Maurano, M. T., Qu, H., Varley, K. E., Gertz, J., Pauli, F., Lee, K., Canfield, T., Weaver, M., Sandstrom, R., et al. (2012) · Genome Research · doi:10.1101/gr.136101.111 · Cited by 588 · cited 4× · see citing works
“The use of DNMT inhibitors, such as 5-azacytidine, were previously used to alter DNA methylation states and infer the influence upon TF binding (Wang et al. 2012; Maurano et al. 2015).”
BackgroundMethodInfluentialHon, G. C., Hawkins, R. D., Caballero, O. L., Lo, C., Lister, R., Pelizzola, M., Valsesia, A., Ye, Z., Kuan, S., Edsall, L. E., et al. (2012) · Genome Research · doi:10.1101/gr.125872.111 · Cited by 583 · see citing works
Self-citationInheritable silencing of endogenous genes by hit-and-run targeted epigenetic editing
Amabile, A., Migliara, A., Capasso, P., Biffi, M., Cittaro, D., Naldini, L., & Lombardo, A. (2016) · Cell · doi:10.1016/j.cell.2016.09.006 · Cited by 516 · see citing works
Competition between DNA methylation and transcription factors determines binding of NRF1
Domcke, S., Bardet, A. F., Adrian Ginno, P., Hartl, D., Burger, L., & Schübeler, D. (2015) · Nature · doi:10.1038/nature16462 · Cited by 508 · see citing works
Rescue of Fragile X Syndrome Neurons by DNA Methylation Editing of the FMR1 Gene
Liu, X. S., Wu, H., Krzisch, M., Wu, X., Graef, J. D., Muffat, J., Hnisz, D., Li, C. H., Yuan, B., Xu, C., et al. (2018) · Cell · doi:10.1016/j.cell.2018.01.012 · Cited by 506 · see citing works
Targeted DNA demethylation in vivo using dCas9–peptide repeat and scFv–TET1 catalytic domain fusions
Morita, S., Noguchi, H., Horii, T., Nakabayashi, K., Kimura, M., Okamura, K., Sakai, A., Nakashima, H., Hata, K., Nakashima, K., et al. (2016) · Nature Biotechnology · doi:10.1038/nbt.3658 · Cited by 496 · see citing works
BS-Seeker2: a versatile aligning pipeline for bisulfite sequencing data
Guo, W., Fiziev, P. P., Yan, W., Cokus, S. J., Sun, X., Zhang, M. Q., Chen, P., & Pellegrini, M. A. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-774 · Cited by 422 · see citing works
Nucleosomes impede Cas9 access to DNA in vivo and in vitro
Horlbeck, M. A., Witkowsky, L. B., Guglielmi, B., Replogle, J. M., Gilbert, L. A., Villalta, J. E., Torigoe, S. E., Tjian, R., & Weissman, J. S. (2016) · eLife · doi:10.7554/elife.12677 · Cited by 415 · see citing works
Brinkman, A. B., Gu, H., Bartels, S. J. J., Zhang, Y., Matarese, F., Simmer, F., Marks, H., Bock, C., Gnirke, A., Meissner, A., et al. (2012) · Genome Research · doi:10.1101/gr.133728.111 · Cited by 413 · see citing works
DNA methylation presents distinct binding sites for human transcription factors
Hu, S., Wan, J., Su, Y., Song, Q., Zeng, Y., Nguyen, H. N., Shin, J., Cox, E., Rho, H. S., Woodard, C., et al. (2013) · eLife · doi:10.7554/elife.00726 · Cited by 349 · see citing works
Efficient targeted DNA methylation with chimeric dCas9–Dnmt3a–Dnmt3L methyltransferase
Stepper, P., Kungulovski, G., Jurkowska, R. Z., Chandra, T., Krueger, F., Reinhardt, R., Reik, W., Jeltsch, A., & Jurkowski, T. P. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1112 · Cited by 326 · see citing works
Role of DNA Methylation in Modulating Transcription Factor Occupancy
Maurano, M. T., Wang, H., John, S., Shafer, A., Canfield, T., Lee, K., & Stamatoyannopoulos, J. A. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.07.024 · Cited by 281 · see citing works
Reprogrammable CRISPR/Cas9-based system for inducing site-specific DNA methylation
McDonald, J. I., Celik, H., Rois, L. E., Fishberger, G., Fowler, T., Rees, R., Kramer, A. C., Martens, A., Edwards, J. R., & Challen, G. A. (2016) · Biology Open · doi:10.1242/bio.019067 · Cited by 275 · see citing works
Structural Basis for the Versatile and Methylation-Dependent Binding of CTCF to DNA
Hashimoto, H., Wang, D., Horton, J. R., Zhang, X., Corces, V. G., & Cheng, X. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.05.004 · Cited by 268 · see citing works
O’Geen, H., Ren, C., Nicolet, C. M., Perez, A. A., Halmai, J. A. N. M., Le, V. M., Mackay, J. P., Farnham, P., & Segal, D. J. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx578 · Cited by 242 · see citing works
Epigenetic reprogramming of cancer cells via targeted DNA methylation
Rivenbark, A. G., Stolzenburg, S., Beltrán, A. S., Yuan, X., Rots, M. G., Strahl, B. D., & Blancafort, P. (2012) · Epigenetics · doi:10.4161/epi.19507 · Cited by 223 · see citing works
Targeted DNA methylation in vivo using an engineered dCas9-MQ1 fusion protein
Lei, Y., Zhang, X., Su, J., Jeong, M., Gundry, M. C., Huang, Y.-H., Zhou, Y., Li, W., & Goodell, M. A. (2017) · Nature Communications · doi:10.1038/ncomms16026 · Cited by 218 · see citing works
DNA epigenome editing using CRISPR-Cas SunTag-directed DNMT3A
Huang, Y., Su, J., Lei, Y., Brunetti, L., Gundry, M. C., Zhang, X., Jeong, M., Li, W., & Goodell, M. A. (2017) · Genome biology · doi:10.1186/s13059-017-1306-z · Cited by 216 · see citing works
Transcription Factor Occupancy Can Mediate Active Turnover of DNA Methylation at Regulatory Regions
Feldmann, A., Ivánek, R., Murr, R., Gaidatzis, D., Burger, L., & Schübeler, D. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003994 · Cited by 215 · see citing works
Statham, A. L., Robinson, M. D., Song, J. Z., Coolen, M. W., Stirzaker, C., & Clark, S. J. (2012) · Genome Research · doi:10.1101/gr.132076.111 · Cited by 208 · see citing works
Briggs, A. W., Rios, X., Chari, R., Yang, L., Zhang, F., Mali, P., & Church, G. M. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks624 · Cited by 207 · see citing works
Siddique, A. N., Nunna, S., Rajavelu, A., Zhang, Y., Jurkowska, R. Z., Reinhardt, R., Rots, M. G., Ragozin, S., Jurkowski, T. P., & Jeltsch, A. (2012) · Journal of Molecular Biology · doi:10.1016/j.jmb.2012.11.038 · Cited by 172 · see citing works
Genome-wide tracking of dCas9-methyltransferase footprints
Galonska, C., Charlton, J., Mattei, A. L., Donaghey, J., Clement, K., Gu, H., Mohammad, A. W., Stamenova, E. K., Cacchiarelli, D., Klages, S., et al. (2018) · Nature Communications · doi:10.1038/s41467-017-02708-5 · Cited by 160 · see citing works
Critical DNA Binding Interactions of the Insulator Protein CTCF
Renda, M., Baglivo, I., Burgess-Beusse, B. L., Esposito, S., Fattorusso, R., Felsenfeld, G., & Pedone, P. V. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m706213200 · Cited by 152 · see citing works
Teif, V. B., Beshnova, D. A., Vainshtein, Y., Marth, C., Mallm, J., Höfer, T., & Rippe, K. (2014) · Genome Research · doi:10.1101/gr.164418.113 · Cited by 151 · see citing works
TALE-mediated epigenetic suppression of CDKN2A increases replication in human fibroblasts
Bernstein, D. L., Lay, J. E. L., Ruano, E. G., & Kaestner, K. H. (2015) · Journal of Clinical Investigation · doi:10.1172/jci77321 · Cited by 137 · see citing works
Chromatin Control of Developmental Dynamics and Plasticity
Perino, M., & Veenstra, G. J. C. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.08.004 · Cited by 131 · see citing works
Nucleosomes Inhibit Cas9 Endonuclease Activity in Vitro
Hinz, J. M., Laughery, M. F., & Wyrick, J. J. (2015) · Biochemistry · doi:10.1021/acs.biochem.5b01108 · Cited by 112 · see citing works
TET‐catalyzed oxidation of intragenic 5‐methylcytosine regulates CTCF‐dependent alternative splicing
Marina, R. J., Sturgill, D. M., Bailly, M. A., Thénoz, M., Varma, G., Prigge, M. F., Nanan, K. K., Shukla, S., Haque, N., & Oberdoerffer, S. (2015) · The EMBO Journal · doi:10.15252/embj.201593235 · Cited by 106 · see citing works
Stolzenburg, S., Beltrán, A. S., Swift‐Scanlan, T., Rivenbark, A. G., Rashwan, R., & Blancafort, P. (2015) · Oncogene · doi:10.1038/onc.2014.470 · Cited by 94 · see citing works
Targeted DNA methylation in human cells using engineered dCas9-methyltransferases
Xiong, T., Meister, G. E., Workman, R. E., Kato, N. C., Spellberg, M. J., Türker, F., Timp, W., Ostermeier, M., & Novina, C. D. (2017) · Scientific Reports · doi:10.1038/s41598-017-06757-0 · Cited by 88 · see citing works
Oligomerization of DNMT3A Controls the Mechanism of de Novo DNA Methylation
Holz-Schietinger, C., Matje, D. M., Harrison, M. F., & Reich, N. O. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.284687 · Cited by 77 · see citing works
Differential peak calling of ChIP-seq signals with replicates with THOR
Allhoff, M., Seré, K., Pires, J. F., Zenke, M., & Costa, I. G. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw680 · Cited by 75 · see citing works
Synthetic epigenetics—towards intelligent control of epigenetic states and cell identity
Jurkowski, T. P., Ravichandran, M., & Stepper, P. (2015) · Clinical Epigenetics · doi:10.1186/s13148-015-0044-x · Cited by 71 · see citing works
Nunna, S., Reinhardt, R., Ragozin, S., & Jeltsch, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087703 · Cited by 65 · see citing works
Ford, E., Grimmer, M. R., Stolzenburg, S., Bogdanovic, O., Mendoza, A. D., Farnham, P. J., Blancafort, P., & Lister, R. (2017) · doi:10.1101/170506 · Cited by 45 · cited 1× · see citing works
“…deposition of DNA methylation (Rivenbark et al. 2012; Siddique et al. 2013; Nunna et al. 2014; Bernstein et al. 2015; Stolzenburg et al. 2015; Stepper et al. 2017; McDonald et al. 2016; Amabile et al. 2016; Liu et al. 2016; O’Geen et al. 2017; Xiong et al. 2017; Lei et al. 2017; Ford et al. 2017).”
BackgroundSelf-citationEpigenetic and genetic deregulation in cancer target distinct signaling pathway domains
Gao, Y., & Teschendorff, A. E. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1100 · Cited by 25 · see citing works
Brave new epigenomes: the dawn of epigenetic engineering
Köferle, A., Stricker, S. H., & Beck, S. (2015) · Genome Medicine · doi:10.1186/s13073-015-0185-8 · Cited by 22 · see citing works
Flagged first, then by citations
2 of the 69 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
The diverse roles of DNA methylation in mammalian development and disease
Greenberg, M., & Bourc’his, D. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0159-6 · Cited by 2,160 · see citing works
Dynamic DNA methylation: In the right place at the right time
Luo, C., Hajkova, P., & Ecker, J. R. (2018) · Science · doi:10.1126/science.aat6806 · Cited by 668 · see citing works
Functions and mechanisms of epigenetic inheritance in animals
Skvortsova, K., Iovino, N., & Bogdanović, O. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0074-2 · Cited by 517 · see citing works
CRISPR technologies for precise epigenome editing
Nakamura, M., Gao, Y., Dominguez, A. A., & Qi, L. S. (2021) · Nature Cell Biology · doi:10.1038/s41556-020-00620-7 · Cited by 446 · see citing works
DNA methylation in mammalian development and disease
Smith, Z. D., Hetzel, S., & Meissner, A. (2024) · Nature Reviews Genetics · doi:10.1038/s41576-024-00760-8 · Cited by 280 · see citing works
Epigenome plasticity in plants
Lloyd, J. P. B., & Lister, R. (2021) · Nature Reviews Genetics · doi:10.1038/s41576-021-00407-y · Cited by 209 · see citing works
Self-citationMechanisms of Interplay between Transcription Factors and the 3D Genome
Kim, S., & Shendure, J. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.08.010 · Cited by 204 · see citing works
Gene editing and CRISPR in the clinic: current and future perspectives
Hirakawa, M. P., Krishnakumar, R., Timlin, J. A., Carney, J. P., & Butler, K. S. (2020) · Bioscience Reports · doi:10.1042/bsr20200127 · Cited by 207 · see citing works
CRISPR-Cas Tools and Their Application in Genetic Engineering of Human Stem Cells and Organoids
Hendriks, D. F. G., Clevers, H. C., & Artegiani, B. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.10.014 · Cited by 196 · see citing works
Enhancer DNA methylation: implications for gene regulation
Angeloni, A., & Bogdanović, O. (2019) · Essays in Biochemistry · doi:10.1042/ebc20190030 · Cited by 176 · see citing works
CRISPR/dCas9 Tools: Epigenetic Mechanism and Application in Gene Transcriptional Regulation
Cai, R., Lv, R., Shi, X., Yang, G., & Jin, J. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241914865 · Cited by 180 · see citing works
Ezh2-dCas9 and KRAB-dCas9 enable engineering of epigenetic memory in a context-dependent manner
O’Geen, H., Bates, S. L., Carter, S., Nisson, K., Halmai, J. A. N. M., Fink, K. D., Rhie, S. K., Farnham, P., & Segal, D. J. (2019) · Epigenetics & Chromatin · doi:10.1186/s13072-019-0275-8 · Cited by 171 · see citing works
CRISPR/dCas-mediated transcriptional and epigenetic regulation in plants
Pan, C., Sretenovic, S., & Qi, Y. (2021) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2020.101980 · Cited by 126 · see citing works
de Mendoza, A., Nguyen, T. V., Ford, E., Poppe, D., Buckberry, S., Pflueger, J., Grimmer, M., Stolzenburg, S., Bogdanović, O., Oshlack, A., et al. (2022) · Genome biology · doi:10.1186/s13059-022-02728-5 · Cited by 123 · see citing works
Self-citationEpigenome editing technologies for discovery and medicine
McCutcheon, S. R., Rohm, D., Iglesias, N., & Gersbach, C. A. (2024) · Nature Biotechnology · doi:10.1038/s41587-024-02320-1 · Cited by 122 · see citing works
Epigenetic gene regulation in plants and its potential applications in crop improvement
Zhang, H., & Zhu, J. (2024) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-024-00769-1 · Cited by 118 · see citing works
Tadić, V., Josipović, G., Zoldoš, V., & Vojta, A. (2019) · Methods · doi:10.1016/j.ymeth.2019.05.003 · Cited by 96 · see citing works
Epigenome engineering: new technologies for precision medicine
Sgro, A., & Blancafort, P. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa1000 · Cited by 96 · see citing works
CRISPR/Cas9 Landscape: Current State and Future Perspectives
Tyumentsev, A. I., Tyumentsev, A. I., & Акимкин, В. Г. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242216077 · Cited by 96 · see citing works
Epigenetic Therapies for Osteoarthritis
Grandi, F. C., & Bhutani, N. (2020) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2020.05.008 · Cited by 85 · see citing works
CRISPR-Based Epigenome Editing: Mechanisms and Applications
Fadul, S. M., Arshad, A., & Mehmood, R. (2023) · Epigenomics · doi:10.2217/epi-2023-0281 · Cited by 78 · see citing works
Gene-Specific Targeting of DNA Methylation in the Mammalian Genome
Urbano, A., Smith, J., Weeks, R. J., & Chatterjee, A. (2019) · Cancers · doi:10.3390/cancers11101515 · Cited by 64 · see citing works
DNA methylation and de-methylation using hybrid site-targeting proteins
Lei, Y., Huang, Y., & Goodell, M. A. (2018) · Genome biology · doi:10.1186/s13059-018-1566-2 · Cited by 64 · see citing works
Multigenerational epigenetic inheritance: One step forward, two generations back
Tuscher, J. J., & Day, J. J. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104591 · Cited by 63 · see citing works
CRISPR/Cas9 Epigenome Editing Potential for Rare Imprinting Diseases: A Review
Syding, L. A., Nickl, P., Kašpárek, P., & Sedláček, R. (2020) · Cells · doi:10.3390/cells9040993 · Cited by 63 · see citing works
Josipović, G., Tadić, V., Klasić, M., Zanki, V., Bečeheli, I., Chung, F. F., Ghantous, A., Keser, T., Madunić, J., Bošković, M., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz709 · Cited by 62 · see citing works
Engineering of Effector Domains for Targeted DNA Methylation with Reduced Off-Target Effects
Hofacker, D. T., Broche, J., Laistner, L., Adam, S., Bashtrykov, P., & Jeltsch, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21020502 · Cited by 62 · see citing works
Toward the Development of Epigenome Editing-Based Therapeutics: Potentials and Challenges
Ueda, J., Yamazaki, T., & Funakoshi, H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054778 · Cited by 60 · see citing works
Epigenome editing for targeted DNA (de)methylation: a new perspective in modulating gene expression
Seem, K., Kaur, S., Kumar, S., & Mohapatra, T. (2024) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2024.2320659 · Cited by 58 · see citing works
Editing the Epigenome to Tackle Brain Disorders
Liu, X. S., & Jaenisch, R. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.10.003 · Cited by 56 · see citing works
Epigenetic editing: Dissecting chromatin function in context
Policarpi, C., Dabin, J., & Hackett, J. A. (2021) · BioEssays · doi:10.1002/bies.202000316 · Cited by 54 · see citing works
Rittiner, J. E., Moncalvo, M., Chiba‐Falek, O., & Kantor, B. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00148 · Cited by 52 · see citing works
Super-Enhancers, Phase-Separated Condensates, and 3D Genome Organization in Cancer
Tang, S., Vijayakumar, U., Zhang, Y., & Fullwood, M. (2022) · Cancers · doi:10.3390/cancers14122866 · Cited by 46 · see citing works
Roth, G. V., Gengaro, I. R., & Qi, L. S. (2024) · Cell chemical biology · doi:10.1016/j.chembiol.2024.07.007 · Cited by 55 · see citing works
DNA Methylation Editing by CRISPR-guided Excision of 5-Methylcytosine
Devesa-Guerra, I., Morales‐Ruíz, T., Pérez-Roldán, J., Parrilla-Doblas, J. T., León, M. D., García‐Ortiz, M. V., Ariza, R. R., & Roldán‐Arjona, T. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2020.02.007 · Cited by 51 · see citing works
Targeting cancer epigenetics with CRISPR-dCAS9: Principles and prospects
Rahman, M. M., & Tollefsbol, T. O. (2020) · Methods · doi:10.1016/j.ymeth.2020.04.006 · Cited by 51 · see citing works
Jang, H. J., Shah, N. M., Maeng, J. H., Liang, Y., Basri, N. L., Ge, J., Qu, X., Mahlokozera, T., Tzeng, S., Williams, R. B., et al. (2024) · Nature Genetics · doi:10.1038/s41588-024-01880-x · Cited by 51 · see citing works
Epigenetic basis and targeting of cancer metastasis
Banerjee, R., Smith, J., Eccles, M. R., Weeks, R. J., & Chatterjee, A. (2021) · Trends in cancer · doi:10.1016/j.trecan.2021.11.008 · Cited by 50 · see citing works
Viable offspring derived from single unfertilized mammalian oocytes
Wei, Y., Yang, C., & Zhao, Z. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2115248119 · Cited by 49 · see citing works
CRISPR–Cas-mediated transcriptional control and epi-mutagenesis
Gardiner, J., Ghoshal, B., Wang, M., & Jacobsen, S. E. (2022) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiac033 · Cited by 46 · see citing works
Stevenson, A. W., Deng, Z., Allahham, A., Prêle, C. M., Wood, F. M., & Fear, M. W. (2021) · Experimental Dermatology · doi:10.1111/exd.14414 · Cited by 46 · see citing works
Livshits, G., & Kalinkovich, A. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102267 · Cited by 43 · see citing works
Li, X., Huang, L., Pan, L., Wang, B., & Pan, L. (2021) · Microbiological Research · doi:10.1016/j.micres.2020.126694 · Cited by 42 · see citing works
CRISPR RNA-guided autonomous delivery of Cas9
Wilkinson, R. A., Martin, C. D., Nemudryi, A. A., & Wiedenheft, B. (2018) · Nature Structural & Molecular Biology · doi:10.1038/s41594-018-0173-y · Cited by 42 · see citing works
The Design and Application of DNA-Editing Enzymes as Base Editors
Rallapalli, K. L., & Komor, A. C. (2023) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-052521-013938 · Cited by 40 · see citing works
Rittiner, J. E., Cumaran, M., Malhotra, S., & Kantor, B. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.1035543 · Cited by 40 · see citing works
Reprogramming the anti-tumor immune response via CRISPR genetic and epigenetic editing
Alves, E., Taifour, S., Dolcetti, R., Chee, J., Nowak, A. K., Gaudieri, S., & Blancafort, P. (2021) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2021.04.009 · Cited by 39 · see citing works
Nguyen, K., Dobrowolski, C. N., Shukla, M., Cho, W., Luttge, B. G., & Karn, J. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1010014 · Cited by 37 · see citing works
Potential application of cell reprogramming techniques for cancer research
Saito, S., Lin, Y., Nakamura, Y., Eckner, R., Wuputra, K., Kuo, K., Lin, C., & Yokoyama, K. K. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2924-7 · Cited by 37 · see citing works
A modular dCas9-based recruitment platform for combinatorial epigenome editing
Swain, T., Pflueger, C., Freytag, S., Poppe, D., Pflueger, J., Nguyen, T. V., Li, J. K., & Lister, R. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad1108 · Cited by 35 · see citing works
Self-citationLiao, C., Liang, X., Ke, Y., Li, Y., Liu, M., Liu, Z.-K., He, L., Guo, Y., Bian, H., Chen, Z., et al. (2022) · Oncogene · doi:10.1038/s41388-022-02213-0 · Cited by 35 · see citing works
CRISPR-Mediated Synergistic Epigenetic and Transcriptional Control
Dominguez, A. A., Chavez, M., Urke, A., Gao, Y., Wang, L., & Qi, L. S. (2022) · The CRISPR Journal · doi:10.1089/crispr.2021.0099 · Cited by 33 · see citing works
Mammalian DNA methylome dynamics: mechanisms, functions and new frontiers
Wei, A., & Wu, H. (2022) · Development · doi:10.1242/dev.182683 · Cited by 33 · see citing works
The Role of Plant DNA Methylation in Development, Stress Response, and Crop Breeding
Qiao, S., Song, W., Hu, W., Wang, F., Liao, A., Tan, W., & SongTao, Y. (2024) · Agronomy · doi:10.3390/agronomy15010094 · Cited by 32 · see citing works
Saunderson, E. A., Encabo, H. H., Devis, J., Rouault‐Pierre, K., Piganeau, M., Bell, C. G., Gribben, J. G., Bonnet, D. A., & Ficz, G. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2300224120 · Cited by 34 · see citing works
Chen, R., Cao, Y., Liu, Y., Zhao, D., Li, J., Cheng, Z., Bi, C., & Zhang, X. (2023) · Nature Communications · doi:10.1038/s41467-023-35919-0 · Cited by 31 · see citing works
Kojima, S., Shiochi, N., Sato, K., Yamaura, M., Ito, T., Yamamura, N., Gotō, N., Odamoto, M., Kobayashi, S., Kimura, T., et al. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac344 · Cited by 30 · see citing works
Wong, C. H., Li, C. H., TONG, J. H. M., Zheng, D., Qi-fang, H., Luo, Z., Lou, U. K., Wang, J., To, K., & Chen, Y. (2022) · Molecular Therapy · doi:10.1016/j.ymthe.2022.01.038 · Cited by 30 · see citing works
Targeted DNA methylation of neurodegenerative disease genes via homology directed repair
Cali, C. P., Park, D. S., & Lee, E. B. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz979 · Cited by 28 · see citing works
Marx, N., Eisenhut, P., Weinguny, M., Klanert, G., & Borth, N. (2022) · Biotechnology Advances · doi:10.1016/j.biotechadv.2022.107924 · Cited by 29 · see citing works
CRISPRepi: a multi-omic atlas for CRISPR-based epigenome editing
Shi, L., Li, S., Zhu, R., Lu, C., Xu, X., Li, C., Huang, X., Zhao, X., Mao, F., & Li, K. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae1039 · Cited by 29 · see citing works
Genome organization in immune cells: unique challenges
Johanson, T. M., Chan, W. F., Keenan, C. R., & Allan, R. S. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0155-2 · Cited by 27 · see citing works
Epigenome editing by CRISPR/Cas9 in clinical settings: possibilities and challenges
Pei, W., Zhang, Y., Yin, T., & Yu, Y. (2019) · Briefings in Functional Genomics · doi:10.1093/bfgp/elz035 · Cited by 27 · see citing works
Immunity and Viral Infections: Modulating Antiviral Response via CRISPR–Cas Systems
Brezgin, S., Kostyusheva, A., Олеговна, Б. Е., Volchkova, E. V., Gegechkori, V., Gordeychuk, I. V., Glebe, D., Kostyushev, D. S., & Chulanov, V. (2021) · Viruses · doi:10.3390/v13071373 · Cited by 27 · see citing works
Programmable genome engineering and gene modifications for plant biodesign
Liu, J., Zhang, R., Chai, N., Su, L., Zheng, Z., Liu, T., Guo, Z., Ma, Y., Xie, Y., Xie, X., et al. (2025) · Plant Communications · doi:10.1016/j.xplc.2025.101427 · Cited by 27 · see citing works
Epigenetic Control of a Local Chromatin Landscape
Chiarella, A. M., Lu, D., & Hathaway, N. A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21030943 · Cited by 31 · see citing works
Innovative Precision Gene‐Editing Tools in Personalized Cancer Medicine
Dai, X., Blancafort, P., Wang, P., Sgro, A., Thompson, E. W., & Ostrikov, K. (2020) · Advanced Science · doi:10.1002/advs.201902552 · Cited by 27 · see citing works
Novel epigenetic molecular therapies for imprinting disorders
Wang, S. E., & Jiang, Y. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02208-7 · Cited by 26 · see citing works
Exploring CRISPR-Cas: The transformative impact of gene editing in molecular biology
Pandey, V. P., Sharma, S., & Pokharel, Y. R. (2025) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2025.102717 · Cited by 29 · see citing works
Live-Animal Epigenome Editing: Convergence of Novel Techniques
Gomez, J. A., Beitnere, U., & Segal, D. J. (2019) · Trends in Genetics · doi:10.1016/j.tig.2019.04.007 · Cited by 25 · see citing works
Li, Z., Xiong, X., & Li, J. (2019) · aBIOTECH · doi:10.1007/s42994-019-00003-z · Cited by 25 · see citing works
Human Organoids as an Emerging Tool for Genome Screenings
Andreatta, F., Hendriks, D. F. G., & Artegiani, B. (2025) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-103023-122327 · Cited by 24 · see citing works
Xu, R., Li, Y., Wu, Y., Liu, X., & Gao, S. (2025) · Trends in Genetics · doi:10.1016/j.tig.2025.05.005 · Cited by 25 · see citing works
Breunig, C., Köferle, A., Neuner, A. M., Wiesbeck, M. F., Baumann, V., & Stricker, S. H. (2020) · Physiological Reviews · doi:10.1152/physrev.00034.2019 · Cited by 24 · see citing works
Gene-Targeted DNA Methylation: Towards Long-Lasting Reprogramming of Gene Expression?
Cortés-Mancera, F., Sarno, F., Goubert, D., & Rots, M. G. (2022) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-11454-0_18 · Cited by 24 · see citing works
Current Approaches to Epigenetic Therapy
Griazeva, E. D., Fedoseeva, D. M., Radion, E. I., Ershov, P. V., Meshkov, I. O., Semyanihina, A. V., Makarova, A. S., Makarov, V. V., Yudin, V. S., Keskinov, A. A., et al. (2023) · Epigenomes · doi:10.3390/epigenomes7040023 · Cited by 23 · see citing works
Applications of CRISPR-Cas in Bioengineering, Biotechnology, and Translational Research
Lau, C. (2018) · The CRISPR Journal · doi:10.1089/crispr.2018.0026 · Cited by 22 · see citing works
Cell-free DNA methylation in the clinical management of lung cancer
Ezegbogu, M. O., Wilkinson, E. J., Reid, G., Rodger, E. J., Brockway, B., Russell‐Camp, T., Kumar, R., & Chatterjee, A. (2024) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2024.03.007 · Cited by 23 · see citing works
Ricci, R., & Colasante, G. (2021) · Developmental Neuroscience · doi:10.1159/000515845 · Cited by 22 · see citing works
Advances and Opportunities in Epigenetic Chemical Biology
Beyer, J. N., Raniszewski, N. R., & Burslem, G. M. (2020) · ChemBioChem · doi:10.1002/cbic.202000459 · Cited by 23 · see citing works
Epigenetic inheritance is gated by naïve pluripotency and Dppa2
Carlini, V., Policarpi, C., & Hackett, J. A. (2022) · The EMBO Journal · doi:10.15252/embj.2021108677 · Cited by 20 · see citing works
Decoding the Mechanisms of Plant Epigenetic Adaptations to Stress
Bashir, H., Samanhudi, S., PARJANTO, P., & Setyawati, A. (2025) · Reviews in Agricultural Science · doi:10.7831/ras.13.2_1 · Cited by 20 · see citing works
Modulating immune cell fate and inflammation through CRISPR-mediated DNA methylation editing
Valcárcel, G., López-Rubio, A. V., Lazarenkov, A., Berenguer, C., Calafell-Segura, J., Rodríguez‐Ubreva, J., Ballestar, E., & Sardina, J. L. (2025) · Science Advances · doi:10.1126/sciadv.adt1644 · Cited by 23 · see citing works
Transcriptional enhancers: from prediction to functional assessment on a genome-wide scale
Tobias, I. C., Abatti, L. E., Moorthy, S. D., Mullany, S., Taylor, T., Khader, N., Filice, M., & Mitchell, J. A. (2020) · Genome · doi:10.1139/gen-2020-0104 · Cited by 20 · see citing works
Chen, Y., Luo, X. L., Kang, R., Cui, K., Ou, J., Zhang, X., & Liang, P. (2023) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2023.07.007 · Cited by 20 · see citing works
Sapozhnikov, D. M., & Szyf, M. (2022) · Nature Protocols · doi:10.1038/s41596-022-00741-3 · Cited by 20 · see citing works
Development of super-specific epigenome editing by targeted allele-specific DNA methylation
Rajaram, N., Kouroukli, A. G., Bens, S., Bashtrykov, P., & Jeltsch, A. (2023) · Epigenetics & Chromatin · doi:10.1186/s13072-023-00515-5 · Cited by 19 · see citing works
DNA methylation shapes the Polycomb landscape during the exit from naive pluripotency
Albert, J. R., Urli, T., Monteagudo, A., Breton, A. L., Sultanova, A., David, A., Scarpa, M., Schulz, M., & Greenberg, M. (2024) · Nature Structural & Molecular Biology · doi:10.1038/s41594-024-01405-4 · Cited by 18 · see citing works
George, J. T., Azhar, M., Aich, M., Sinha, D., Ambi, U. B., Maiti, S., Chakraborty, D., & Srivatsan, S. G. (2020) · Journal of the American Chemical Society · doi:10.1021/jacs.0c06541 · Cited by 19 · see citing works
Chromatin Manipulation and Editing: Challenges, New Technologies and Their Use in Plants
Fal, K., Tomková, D., Vachon, G., Chabouté, M., Berr, A., & Carles, C. C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22020512 · Cited by 19 · see citing works
Sapozhnikov, D. M., & Szyf, M. (2023) · Biomedicines · doi:10.3390/biomedicines11051238 · 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
RNA variant assessment using transactivation and transdifferentiation
Nicolas-Martinez, E. C., Robinson, O., Pflueger, C., Gardner, A. E., Corbett, M. A., Ritchie, T., Kroes, T., van Eyk, C. L., Scheffer, I. E., Hildebrand, M. S., et al. (2024) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2024.06.018 · Cited by 18 · see citing works
Self-citationCRISPR-mediated promoter de/methylation technologies for gene regulation
Sung, C. K., & Yim, H. (2020) · Archives of Pharmacal Research · doi:10.1007/s12272-020-01257-8 · Cited by 18 · see citing works
CRISPR activation and interference as investigative tools in the cardiovascular system
Carroll, M. S., & Giacca, M. (2022) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2022.106348 · Cited by 19 · see citing works
Rinonos, S. Z., Li, T., Pianka, S. T., Prins, T. J., Eldred, B. S. C., Kevan, B. M., Liau, L. M., Nghiemphu, P. L., Cloughesy, T. F., & Lai, A. (2024) · Journal of Neuro-Oncology · doi:10.1007/s11060-023-04531-z · Cited by 17 · see citing works
CRISPR/Cas9 in epigenetics studies of health and disease
Sar, P., & Dalai, S. K. (2021) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2021.01.022 · Cited by 17 · see citing works
Locus-Specific DNA Methylation Editing in Melanoma Cell Lines Using a CRISPR-Based System
Smith, J., Banerjee, R., Waly, R., Urbano, A., Gimenez, G., Day, R. C., Eccles, M. R., Weeks, R. J., & Chatterjee, A. (2021) · Cancers · doi:10.3390/cancers13215433 · Cited by 17 · see citing works
Kayabölen, A., Akcan, U., Özturan, D., Polat, H. Ü., Şahin, G. N., Degirmenci, N. P., Bayraktar, C., Söyler, G., Sarayloo, E., Nurtop, E., et al. (2022) · Advanced Science · doi:10.1002/advs.202201294 · Cited by 14 · see citing works
Genomic Targeting of TET Activity for Targeted Demethylation Using CRISPR/Cas9
Nguyen, T. V., & Lister, R. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1294-1_10 · Cited by 16 · see citing works
Self-citation
- Authors
- Pflueger, C., Tan, D., Swain, T., Nguyen, T., Pflueger, J., Nefzger, C., Polo, J. M., Ford, E., & Lister, R.
- Affiliations
- The University of Western Australia (AU)
- Australian Regenerative Medicine Institute (AU)
- Corresponding author
- Ford, Ethan
- Lister, Ryan
- ORCID
- Venue
- Genome Research
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2018-06-15
- Volume
- 28
- Issue
- 8
- Pages
- 1193-1206
- ISSN
- 1088-9051 (ISSN-L)
- 1549-5469
- PMC
- PMC6071642
- OpenAlex
- W2952920376
- Cited by
- 188
- References
- 69
- Citations by year
- 2026: 16 · 2025: 27 · 2024: 28 · 2023: 19 · 2022: 28 · 2021: 21 · 2020: 22 · 2019: 18 · 2018: 9
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genome Research (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- Monash University Research Portal (Monash University) (publishedVersion, other-oa)
- UWA Profiles and Research Repository (UWA) (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion, cc-by-nc)
- HighWire Press Open Archive (submittedVersion)
- Funders
- Australian National Health
- Medical Research Council (GNT1069830)
- Australian Research Council (CE140100008, FT120100862)
- National Institutes of Health (5R01DA036906)
- Raine Medical Research Foundation
- Sylvia and Charles Viertel Senior Medical Research Fellowships
- Howard Hughes Medical Institute
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
- Keywords
- epigenome editing, DNA methylation, dCas9, DNMT3A, SunTag, off-target effects, CTCF, NRF1, chromatin binding, transcriptional regulation
- MeSH terms
- Gene Editing, DNA Methyltransferase 3A, Binding Sites, Chromatin, DNA (Cytosine-5-)-Methyltransferases, Promoter Regions, Genetic, Protein Binding, Recombinant Fusion Proteins, DNA Methylation, Catalytic Domain, Epigenesis, Genetic, CRISPR-Cas Systems
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
