In vivo locus-specific editing of the neuroepigenome
Open accessAbstract
Studies over the past several decades have identified numerous epigenetic mechanisms associated with pathological states in psychiatric and neurological disease. Until recently, studies investigating chromatin-regulatory proteins, using overexpression or knockdown approaches, did not establish causal roles for epigenetic modifications at specific genes because these techniques typically affect hundreds or thousands of genomic loci. In this Review, we describe recent efforts in using locus-specific neuroepigenome editing in vivo to, for the first time, define causal relationships between a single chromatin modification at a specific gene in a defined cell population and downstream measures at the molecular, cellular, circuit and behavioural levels. We briefly introduce three epigenome-editing platforms: zinc-finger proteins, transcriptional activator-like effectors and clustered regularly interspaced short palindromic repeats (CRISPR). We then explore the development of in vivo neuroepigenome-editing tools and their applications to resolve epigenetic contributions to the pathophysiology of brain diseases. We also discuss technical considerations for in vivo neuroepigenome-editing experiments and ongoing innovations in the field, including new tools to investigate chromatin marks, manipulate chromatin topology and induce epigenetic modifications at multiple genes in the same cell. Lastly, we explore the potential clinical applications of in vivo neuroepigenome editing for treating brain pathology.
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?
Cell-type-specific expression of epigenetic modifiers (e.g., histone acetylation or methylation proteins) fused to dCas9 can be made inducible by Cre recombinase, which can be transgenically or virally co-expressed.
“The cell-type-specific expression of epigenetic modifiers (e.g., histone acetylation or methylation proteins) fused to dCas9 are then inducible by Cre recombinase, which can be transgenically or virally co-expressed [155, 156].”
From Cell-type-specific epigenetic effects of early life stress on the brain (2022) · cites this paper as [156]
Determining whether epigenetic modifications at select loci are causal mechanisms of behavior may only be possible by altering target epigenetic modifications in vivo.
“Interpretational challenges also extend to determining whether epigenetic modifications at select loci are ‘causal’ mechanisms of behavior, which may only be possible by altering target epigenetic modifications in vivo [155–157].”
From Cell-type-specific epigenetic effects of early life stress on the brain (2022) · cites this paper as [156]
Tools used for cell-type-specific epigenetic editing include zinc-finger proteins, which can be fused with histone modifiers and target specific DNA sequences, and transcriptional activator-like effectors (TALEs), DNA binding proteins from bacteria that can be targeted to regulate gene transcription.
“Tools used for cell-type-specific epigenetic editing include zinc-finger proteins, which can be fused with histone modifiers and target specific DNA sequences, and transcriptional activator-like effectors (TALEs), DNA binding proteins from bacteria that can be targeted to regulate gene transcription (see review [156]).”
From Cell-type-specific epigenetic effects of early life stress on the brain (2022) · cites this paper as [156]
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
Multiplex Genome Engineering Using CRISPR/Cas Systems
Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., Marraffini, L. A., et al. (2013) · Science · doi:10.1126/science.1231143 · Cited by 15,339 · see citing works
Jenuwein, T., & Allis, C. D. (2001) · Science · doi:10.1126/science.1063127 · Cited by 9,756 · 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
Development and Applications of CRISPR-Cas9 for Genome Engineering
Hsu, P. D., Lander, E. S., & Zhang, F. (2014) · Cell · doi:10.1016/j.cell.2014.05.010 · Cited by 5,762 · see citing works
Chen, X., Xiu, M., Xing, J., Yu, S., Min, D., & Guo, F. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000479439 · Cited by 5,759 · 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 · see citing works
CRISPR-Mediated Modular RNA-Guided Regulation of Transcription in Eukaryotes
Gilbert, L. A., Larson, M. H., Morsut, L., Liu, Z., Brar, G. A., Torres, S. E., Stern-Ginossar, N., Brandman, O., Whitehead, E. H., Doudna, J. A., et al. (2013) · Cell · doi:10.1016/j.cell.2013.06.044 · Cited by 3,696 · see citing works
DNA methylation landscapes: Provocative insights from epigenomics
Suzuki, M. M., & Bird, A. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2341 · Cited by 3,039 · see citing works
Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex
Konermann, S., Brigham, M. D., Trevino, A. E., Joung, J., Abudayyeh, O. O., Barcena, C., Hsu, P. D., Habib, N., Gootenberg, J. S., Nishimasu, H., et al. (2015) · Nature · doi:10.1038/nature14136 · Cited by 2,825 · see citing works
Neurodegenerative Disorders: Parkinson's Disease and Huntington's Disease
Hague, S., Klaffke, S., & Bandmann, O. (2006) · IMPERIAL COLLEGE PRESS eBooks · doi:10.1142/9781860948961_0007 · Cited by 2,767 · see citing works
Evolution and classification of the CRISPR–Cas systems
Makarova, K. S., Haft, D. H., Barrangou, R., Brouns, S. J. J., Charpentier, E., Horvath, P., Moineau, S., Mojica, F. J. M., Wolf, Y. I., Yakunin, A. F., et al. (2011) · Nature Reviews Microbiology · doi:10.1038/nrmicro2577 · Cited by 2,512 · see citing works
Rationally engineered Cas9 nucleases with improved specificity
Slaymaker, I. M., Gao, L., Zetsche, B., Scott, D. A., Yan, W. X., & Zhang, F. (2016) · Science · doi:10.1126/science.aad5227 · Cited by 2,414 · see citing works
Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain.
Kim, Y. G., Cha, J., & Chandrasegaran, S. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.3.1156 · Cited by 2,099 · see citing works
Improving CRISPR-Cas nuclease specificity using truncated guide RNAs
Fu, Y., Sander, J. D., Reyon, D., Cascio, V. M., & Joung, J. K. (2014) · Nature Biotechnology · doi:10.1038/nbt.2808 · Cited by 1,993 · see citing works
A Simple Cipher Governs DNA Recognition by TAL Effectors
Moscou, M., & Bogdanove, A. J. (2009) · Science · doi:10.1126/science.1178817 · Cited by 1,992 · see citing works
Hilton, I. B., D’Ippolito, A. M., Vockley, C. M., Thakore, P. I., Crawford, G. E., Reddy, T. E., & Gersbach, C. A. (2015) · Nature Biotechnology · doi:10.1038/nbt.3199 · Cited by 1,879 · see citing works
Chan, K. Y., Jang, M. J., Yoo, B. B., Greenbaum, A., Ravi, N., Wu, W.-L., Sánchez-Guardado, L., Lois, C., Mazmanian, S. K., Deverman, B. E., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4593 · Cited by 1,578 · 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 1,559 · see citing works
Evolved Cas9 variants with broad PAM compatibility and high DNA specificity
Hu, J. H., Miller, S. M., Geurts, M. H., Tang, W., Chen, L., Sun, N., Zeina, C. M., Gao, X., Rees, H. A., Lin, Z., et al. (2018) · Nature · doi:10.1038/nature26155 · Cited by 1,552 · see citing works
Structure and function of long noncoding RNAs in epigenetic regulation
Mercer, T. R., & Mattick, J. S. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2480 · Cited by 1,436 · see citing works
Gene Editing of <i>CCR5</i> in Autologous CD4 T Cells of Persons Infected with HIV
Tebas, P., Stein, D., Tang, W. W., Frank, I., Wang, S. Q., Lee, G., Spratt, S. K., Surosky, R. T., Giedlin, M. A., Nichol, G., et al. (2014) · New England Journal of Medicine · doi:10.1056/nejmoa1300662 · Cited by 1,357 · see citing works
CRISPR RNA–guided activation of endogenous human genes
Maeder, M. L., Linder, S. J., Cascio, V. M., Fu, Y., Ho, Q. H., & Joung, J. K. (2013) · Nature Methods · doi:10.1038/nmeth.2598 · Cited by 1,249 · 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 · see citing works
Transcriptional and epigenetic mechanisms of addiction
Robison, A. J., & Nestler, E. J. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3111 · Cited by 993 · see citing works
Self-citationDeep sequencing reveals 50 novel genes for recessive cognitive disorders
Najmabadi, H., Hu, H., Garshasbi, M., Zemojtel, T., Abedini, S. S., Chen, W., Hosseini, M., Behjati, F., Haas, S., Jamali, P., et al. (2011) · Nature · doi:10.1038/nature10423 · Cited by 965 · see citing works
Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells
Wu, X., Scott, D. A., Kriz, A. J., Chiu, A. C., Hsu, P. D., Dadon, D. B., Cheng, A. W., Trevino, A. E., Konermann, S., Chen, S., et al. (2014) · Nature Biotechnology · doi:10.1038/nbt.2889 · Cited by 944 · see citing works
Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds
Zalatan, J. G., Lee, M. E., Almeida, R., Gilbert, L. A., Whitehead, E. H., La Russa, M., Tsai, J. C., Weissman, J. S., Dueber, J. E., Qi, L. S., et al. (2015) · Cell · doi:10.1016/j.cell.2014.11.052 · Cited by 938 · see citing works
Daigle, T. L., Madisen, L., Hage, T. A., Valley, M. T., Knoblich, U., Larsen, R. S., Takeno, M. M., Huang, L., Gu, H., Larsen, R., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.035 · Cited by 817 · see citing works
Optical control of mammalian endogenous transcription and epigenetic states
Konermann, S., Brigham, M. D., Trevino, A. E., Hsu, P. D., Heidenreich, M., Cong, L., Platt, R. J., Scott, D. A., Church, G. M., & Zhang, F. (2013) · Nature · doi:10.1038/nature12466 · Cited by 803 · 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
Chromatin Remodeling Is a Key Mechanism Underlying Cocaine-Induced Plasticity in Striatum
Kumar, A., Choi, K.-H., Renthal, W., Tsankova, N. M., Theobald, D. E. H., Truong, H.-T., Russo, S. J., LaPlant, Q., Sasaki, T. S., Whistler, K. N., et al. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.023 · Cited by 764 · see citing works
Self-citationCheng, A. W., Wang, H., Yang, H., Shi, L., Yarden Katz, A., Theunissen, T. W., Rangarajan, S., Shivalila, C., Dadon, D. B., & Jaenisch, R. (2013) · Cell Research · doi:10.1038/cr.2013.122 · Cited by 743 · see citing works
Genome-editing Technologies for Gene and Cell Therapy
Maeder, M. L., & Gersbach, C. A. (2016) · Molecular Therapy · doi:10.1038/mt.2016.10 · Cited by 722 · see citing works
Essential Role of the Histone Methyltransferase G9a in Cocaine-Induced Plasticity
Maze, I., Covington, H. E., Dietz, D. M., LaPlant, Q., Renthal, W., Russo, S. J., Mechanic, M., Mouzon, E., Neve, R. L., Haggarty, S. J., et al. (2010) · Science · doi:10.1126/science.1179438 · Cited by 665 · see citing works
Self-citationFunctional annotation of native enhancers with a Cas9–histone demethylase fusion
Kearns, N. A., Pham, H., Tabak, B., Genga, R. M., Silverstein, N. J., Garber, M., & Maehr, R. (2015) · Nature Methods · doi:10.1038/nmeth.3325 · Cited by 656 · see citing works
A light-inducible CRISPR-Cas9 system for control of endogenous gene activation
Polstein, L. R., & Gersbach, C. A. (2015) · Nature Chemical Biology · doi:10.1038/nchembio.1753 · Cited by 630 · 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
Regulation of gene expression and cocaine reward by CREB and ΔFosB
McClung, C. A., & Nestler, E. J. (2003) · Nature Neuroscience · doi:10.1038/nn1143 · Cited by 625 · see citing works
Self-citationRescue 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
Histone serotonylation is a permissive modification that enhances TFIID binding to H3K4me3
Farrelly, L. A., Thompson, R. E., Zhao, S., Lepack, A. E., Lyu, Y., Bhanu, N. V., Zhang, B., Loh, Y. E., Ramakrishnan, A., Vadodaria, K. C., et al. (2019) · Nature · doi:10.1038/s41586-019-1024-7 · Cited by 478 · see citing works
Improved CUT&RUN chromatin profiling tools
Meers, M. P., Bryson, T. D., Henikoff, J. G., & Henikoff, S. (2019) · eLife · doi:10.7554/elife.46314 · Cited by 474 · see citing works
Cornerstones of CRISPR–Cas in drug discovery and therapy
Fellmann, C., Gowen, B. G., Lin, P., Doudna, J. A., & Corn, J. E. (2016) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2016.238 · Cited by 442 · see citing works
Kügler, S., Kilic, E., & Bähr, M. (2003) · Gene Therapy · doi:10.1038/sj.gt.3301905 · Cited by 412 · see citing works
Genome-wide Analysis of Chromatin Regulation by Cocaine Reveals a Role for Sirtuins
Renthal, W., Kumar, A., Xiao, G., Wilkinson, M., Covington, H. E., Maze, I., Sikder, D., Robison, A. J., LaPlant, Q., Dietz, D. M., et al. (2009) · Neuron · doi:10.1016/j.neuron.2009.03.026 · Cited by 409 · see citing works
Self-citationAnti-CRISPR: discovery, mechanism and function
Pawluk, A., Davidson, A. R., & Maxwell, K. L. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2017.120 · Cited by 398 · see citing works
Lee, B., Lee, K., Panda, S., Gonzales-Rojas, R., Chong, A., Bugay, V., Park, H. M., Brenner, R., Murthy, N., & Lee, H. Y. (2018) · Nature Biomedical Engineering · doi:10.1038/s41551-018-0252-8 · Cited by 361 · see citing works
Increasing the specificity of CRISPR systems with engineered RNA secondary structures
Kocak, D. D., Josephs, E. A., Bhandarkar, V., Adkar, S. S., Kwon, J. B., & Gersbach, C. A. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0095-1 · Cited by 351 · see citing works
Dreier, B., Beerli, R. R., Segal, D. J., Flippin, J. D., & Barbas, C. F. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m102604200 · Cited by 329 · 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
In vivo Perturb-Seq reveals neuronal and glial abnormalities associated with autism risk genes
Jin, X., Simmons, S. K., Guo, A., Shetty, A. S., Ko, M., Nguyen, L., Jokhi, V., Robinson, E., Oyler, P., Curry, N., et al. (2020) · Science · doi:10.1126/science.aaz6063 · Cited by 317 · see citing works
The role of DNA methylation in stress-related psychiatric disorders
Klengel, T., Pape, J., Binder, E. B., & Mehta, D. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.01.013 · Cited by 309 · see citing works
Cyclin-dependent kinase 5 governs learning and synaptic plasticity via control of NMDAR degradation
Hawasli, A. H., Benavides, D. R., Nguyen, C. T. N., Kansy, J. W., Hayashi, K., Chambon, P., Greengard, P., Powell, C. M., Cooper, D., & Bibb, J. A. (2007) · Nature Neuroscience · doi:10.1038/nn1914 · Cited by 292 · see citing works
A Role for Repressive Histone Methylation in Cocaine-Induced Vulnerability to Stress
Covington, H. E., Maze, I., Sun, H., Bomze, H. M., DeMaio, K. D., Wu, E. Y., Dietz, D. M., Lobo, M. K., Ghose, S., Mouzon, E., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.06.007 · Cited by 289 · see citing works
Self-citationApplications of CRISPR–Cas systems in neuroscience
Heidenreich, M., & Zhang, F. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn.2015.2 · Cited by 282 · see citing works
Manipulation of nuclear architecture through CRISPR-mediated chromosomal looping
Morgan, S. L., Mariano, N. C., Bermudez, A., Arruda, N. L., Wu, F., Luo, Y., Shankar, G., Jia, L., Chen, H., Hu, J.-F., et al. (2017) · Nature Communications · doi:10.1038/ncomms15993 · Cited by 279 · see citing works
Zhou, H., Liu, J., Zhou, C., Gao, N., Rao, Z., Li, H., Hu, X., Li, C., Yao, X., Shen, X., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-017-0060-6 · Cited by 276 · see citing works
Locus-specific histone deacetylation using a synthetic CRISPR-Cas9-based HDAC
Kwon, D. Y., Zhao, Y.-T., Lamonica, J. M., & Zhou, Z. (2017) · Nature Communications · doi:10.1038/ncomms15315 · Cited by 246 · see citing works
Lobo, M. K., Zaman, S., Damez-Werno, D. M., Koo, J. W., Bagot, R. C., DiNieri, J. A., Nugent, A., Finkel, E., Chaudhury, D., Chandra, R., et al. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1875-13.2013 · Cited by 245 · see citing works
Self-citationAnti-CRISPR protein applications: natural brakes for CRISPR-Cas technologies
Marino, N. D., Pinilla‐Redondo, R., Csörgő, B., & Bondy‐Denomy, J. (2020) · Nature Methods · doi:10.1038/s41592-020-0771-6 · Cited by 240 · see citing works
Locus-specific epigenetic remodeling controls addiction- and depression-related behaviors
Heller, E. A., Cates, H. M., Peña, C. J., Sun, H., Shao, N., Feng, J., Golden, S. A., Herman, J. P., Walsh, J. J., Mazei-Robison, M., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3871 · Cited by 227 · see citing works
Self-citationTargeted 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
The Discovery, Mechanisms, and Evolutionary Impact of Anti-CRISPRs
Borges, A. L., Davidson, A. R., & Bondy‐Denomy, J. (2017) · Annual Review of Virology · doi:10.1146/annurev-virology-101416-041616 · Cited by 215 · see citing works
CRISPR-Mediated Programmable 3D Genome Positioning and Nuclear Organization
Wang, H., Xu, X., Nguyen, C. M., Liu, Y., Gao, Y., Lin, X., Daley, T., Kipniss, N. H., Russa, M. F. L., & Qi, L. S. (2018) · Cell · doi:10.1016/j.cell.2018.09.013 · Cited by 215 · see citing works
Шевцова, З. І., Malik, I., Michel, U., Bähr, M., & Kügler, S. (2004) · Experimental Physiology · doi:10.1113/expphysiol.2004.028159 · Cited by 207 · see citing works
Epigenetic editing of the Dlg4/PSD95 gene improves cognition in aged and Alzheimer’s disease mice
Bustos, F. J., Ampuero, E., Jury, N., Aguilar, R., Falahi, F., Toledo, J. A., Ahumada, J., Lata, J., Cubillos, P., Henríquez, B., et al. (2017) · Brain · doi:10.1093/brain/awx272 · Cited by 205 · see citing works
Phenotypic Landscape of Schizophrenia-Associated Genes Defines Candidates and Their Shared Functions
Thyme, S. B., Pieper, L. M., Li, E. H., Pandey, S., Wang, Y., Morris, N. S., Sha, C., Choi, J. W., Herrera, K. J., Soucy, E. R., et al. (2018) · Cell · doi:10.1016/j.cell.2019.01.048 · Cited by 205 · see citing works
CRISPR Activation Screens Systematically Identify Factors that Drive Neuronal Fate and Reprogramming
Liu, Y., Chen, Y., Daley, T., Wang, F., Cao, W., Bhate, S. S., Lin, X., Still, C., Liu, H., Zhao, D., et al. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.09.003 · Cited by 204 · see citing works
Zinc Fingers: A Novel Protein Fold for Nucleic Acid RecognitionPreprint
Klug, A., & Rhodes, D. (1987) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1987.052.01.054 · Cited by 180 · see citing works
RNA-guided transcriptional silencing in vivo with S. aureus CRISPR-Cas9 repressors
Thakore, P. I., Kwon, J. B., Nelson, C. E., Rouse, D. C., Gemberling, M. P., Oliver, M. L., & Gersbach, C. A. (2018) · Nature Communications · doi:10.1038/s41467-018-04048-4 · Cited by 173 · 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 interference-based specific and efficient gene inactivation in the brain
Zheng, Y., Shen, W., Zhang, J., Yang, B., Liu, Y., Qi, H., Yu, X., Lu, S., Chen, Y., Xu, Y., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0077-5 · Cited by 157 · see citing works
Chen, L., Lin, Y. T., Gallegos, D. A., Hazlett, M. F., Gómez-Schiavon, M., Yang, M. G., Kalmeta, B., Zhou, A. S., Holtzman, L., Gersbach, C. A., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.01.032 · Cited by 157 · see citing works
Role of DNA Methylation in the Nucleus Accumbens in Incubation of Cocaine Craving
Massart, R., Barnea, R., Dikshtein, Y., Suderman, M. J., Meir, O., Hallett, M. T., Kennedy, P., Nestler, E. J., Moshe Szyf, A., & Yadid, G. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3053-14.2015 · Cited by 150 · see citing works
Self-citationSingle-Cell RNA Sequencing: Unraveling the Brain One Cell at a Time
Ofengeim, D., Γιαγτζόγλου, Ν., Huh, D., Zou, C., & Yuan, J. (2017) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2017.04.006 · Cited by 146 · see citing works
A Neuron-Optimized CRISPR/dCas9 Activation System for Robust and Specific Gene Regulation
Savell, K. E., Bach, S. V., Zipperly, M. E., Revanna, J. S., Goska, N. A., Tuscher, J. J., Duke, C. G., Sultan, F. A., Burke, J. N., Williams, D., et al. (2019) · eNeuro · doi:10.1523/eneuro.0495-18.2019 · Cited by 138 · see citing works
Moreno, A. M., Palmer, N. D., Alemán, F., Chen, G., Pla, A., Jiang, N. J., Chew, W. L., Law, M., & Mali, P. (2019) · Nature Biomedical Engineering · doi:10.1038/s41551-019-0431-2 · Cited by 128 · see citing works
Engineering Delivery Vehicles for Genome Editing
Nelson, C. E., & Gersbach, C. A. (2016) · Annual Review of Chemical and Biomolecular Engineering · doi:10.1146/annurev-chembioeng-080615-034711 · Cited by 118 · see citing works
Hamilton, P. J., Burek, D. J., Lombroso, S. I., Neve, R. L., Robison, A. J., Nestler, E. J., & Heller, E. A. (2018) · Neuropsychopharmacology · doi:10.1038/npp.2017.88 · Cited by 113 · see citing works
Self-citationStress resilience is promoted by a Zfp189-driven transcriptional network in prefrontal cortex
Lorsch, Z. S., Hamilton, P. J., Ramakrishnan, A., Parise, E. M., Salery, M., Wright, W. J., Lepack, A. E., Mews, P., Issler, O., McKenzie, A. T., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0462-8 · Cited by 111 · see citing works
Self-citationHeller, E. A., Hamilton, P. J., Burek, D. D., Lombroso, S. I., Peña, C. J., Neve, R. L., & Nestler, E. J. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.0013-16.2016 · Cited by 109 · see citing works
Self-citationAdvancing chimeric antigen receptor T cell therapy with CRISPR/Cas9
Ren, J., & Zhao, Y. (2017) · Protein & Cell · doi:10.1007/s13238-017-0410-x · Cited by 101 · see citing works
The emerging role of 5-hydroxymethylcytosine in neurodegenerative diseases
Al‐Mahdawi, S., Virmouni, S. A., & Pook, M. A. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00397 · Cited by 100 · see citing works
Cdk5 Modulates Cocaine Reward, Motivation, and Striatal Neuron Excitability
Benavides, D. R., Quinn, J. J., Zhong, P., Hawasli, A. H., Dileone, R., Kansy, J. W., Olausson, P., Yan, Z., Taylor, J. R., & Bibb, J. A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4061-07.2007 · Cited by 97 · see citing works
Neuron-Specific Genome Modification in the Adult Rat Brain Using CRISPR-Cas9 Transgenic Rats
Bäck, S., Necarsulmer, J., Ramsey, L. A., Coke, L. M., Koivula, P. P., Heathward, E. J., Fortuno, L. V., Zhang, Y., Yeh, C., Baldwin, H. A., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.01.035 · Cited by 92 · see citing works
Nr4a1 suppresses cocaine-induced behavior via epigenetic regulation of homeostatic target genes
Carpenter, M. D., Hu, Q., Bond, A. M., Lombroso, S. I., Czarnecki, K. S., Lim, C. J., Song, H., Wimmer, M. E., Pierce, R. C., & Heller, E. A. (2020) · Nature Communications · doi:10.1038/s41467-020-14331-y · Cited by 92 · see citing works
Herpes simplex virus-mediated gene transfer as a tool for neuropsychiatric research
Carlezon, Jr., Nestler, E. J., & Neve, R. L. (2000) · Critical Reviews™ in Neurobiology · doi:10.1615/critrevneurobiol.v14.i1.30 · Cited by 90 · see citing works
Self-citation“The free market” and the Asian crisis
Jones, G. (2000) · Critical Review · doi:10.1080/08913810008443546 · Cited by 85 · see citing works
Cell-Type-Specific Role of ΔFosB in Nucleus Accumbens In Modulating Intermale Aggression
Aleyasin, H., Flanigan, M. E., Golden, S. A., Takahashi, A., Ménard, C., Pfau, M. L., Multer, J., Pina, J., McCabe, K. A., Bhatti, N., et al. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0296-18.2018 · Cited by 80 · see citing works
Self-citationSafe and stable noninvasive focal gene delivery to the mammalian brain following focused ultrasound
Stavarache, M. A., Petersen, N., Jurgens, E. M., Milstein, E. R., Rosenfeld, Z. B., Ballon, D. J., & Kaplitt, M. G. (2019) · Journal of Neurosurgery · doi:10.3171/2017.8.jns17790 · Cited by 76 · see citing works
Laganière, J., Kells, A. P., Lai, J. T., Guschin, D. Y., Paschon, D. E., Meng, X., Fong, L. K., Yu, Q., Rebar, E. J., Gregory, P. D., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2440-10.2010 · Cited by 72 · see citing works
Evolution of Programmable Zinc Finger-recombinases with Activity in Human Cells
Gordley, R. M., Smith, J., Gräslund, T., & Barbas, C. F. (2007) · Journal of Molecular Biology · doi:10.1016/j.jmb.2007.01.017 · Cited by 68 · see citing works
Engmann, O., Labonté, B., Mitchell, A., Bashtrykov, P., Calipari, E. S., Rosenbluh, C., Loh, Y. E., Walker, D. M., Burek, D., Hamilton, P. J., et al. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.04.013 · Cited by 62 · see citing works
Self-citationMerienne, N., Douce, J. L., Faivre, E., Déglon, N., & Bonvento, G. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00106 · Cited by 58 · see citing works
Peter, C. J., Saito, A., Hasegawa, Y., Tanaka, Y., Nagpal, M., Perez, G., Alway, E., Espeso‐Gil, S., Fayyad, T., Ratner, C., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12013-y · 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
Cyclin-Dependent Kinase 5 in the Ventral Tegmental Area Regulates Depression-Related Behaviors
Zhong, P., Liu, X., Zhang, Z., Hu, Y. C., Liu, S. J., Lezama-Ruiz, M., Joksimovic, M., & Liu, Q.-S. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3673-13.2014 · Cited by 53 · see citing works
Locus-specific DNA methylation of Mecp2 promoter leads to autism-like phenotypes in mice
Lu, Z., Liu, Z., Mao, W., Wang, X., Zheng, X., Chen, S., Cao, B., Huang, S., Zhang, X., Zhou, T., et al. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-2290-x · Cited by 52 · 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
Kolb, A. F., Coates, C. J., Kaminski, J., Summers, J. B., Miller, A. D., & Segal, D. J. (2005) · Trends in biotechnology · doi:10.1016/j.tibtech.2005.06.005 · Cited by 47 · see citing works
Critical Parameters for Genome Editing Using Zinc Finger Nucleases
Camenisch, T. D., Brilliant, M. H., & Segal, D. J. (2008) · Mini-Reviews in Medicinal Chemistry · doi:10.2174/138955708784567458 · Cited by 44 · see citing works
Rational design of a compact CRISPR-Cas9 activator for AAV-mediated delivery
Vora, S., Cheng, J., Xiao, R., VanDusen, N. J., Quintino, L., Pu, W. T., Vandenberghe, L. H., Chavez, A., & Church, G. (2018) · doi:10.1101/298620 · Cited by 42 · see citing works
Sex-Specific Regulation of Fear Memory by Targeted Epigenetic Editing of Cdk5
Sase, A., Lombroso, S. I., Santhumayor, B. A., Wood, R. R., Lim, C. J., Neve, R. L., & Heller, E. A. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.11.022 · Cited by 40 · see citing works
Cates, H. M., Heller, E. A., Lardner, C. K., Purushothaman, I., Peña, C. J., Walker, D. M., Cahill, M. E., Neve, R. L., Shen, L., Bagot, R. C., et al. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.11.027 · Cited by 39 · see citing works
Self-citationSTEM CELL THERAPIES, GENE-BASED THERAPIES, OPTOGENETICS, AND RETINAL PROSTHETICS:
Wood, E. H., Tang, P. H., la Huerta, I. D., Korot, E., Muscat, S. P., Palanker, D., & Williams, G. A. (2019) · Retina · doi:10.1097/iae.0000000000002449 · Cited by 32 · see citing works
Hamilton, P. J., Lim, C. J., Nestler, E. J., & Heller, E. A. (2018) · Methods in Molecular Biology · doi:10.1007/978-1-4939-7774-1_5 · Cited by 28 · see citing works
Self-citationSu, S. C., Rudenko, A., Cho, S., & Tsai, L. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.06.016 · Cited by 24 · see citing works
Viral Expression of Epigenome Editing Tools in Rodent Brain Using Stereotaxic Surgery Techniques
Hamilton, P. J., Lim, C. J., Nestler, E. J., & Heller, E. A. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7774-1_10 · Cited by 19 · see citing works
Self-citationBlankvoort, S., Descamps, L. A. L., & Kentros, C. G. (2020) · Neuroscience Research · doi:10.1016/j.neures.2020.01.009 · Cited by 19 · see citing works
In vivo Perturb-Seq reveals neuronal and glial abnormalities associated with Autism risk genesPreprint
Jin, X., Simmons, S., Guo, A. X., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/791525 · Cited by 15 · see citing works
Genetic and epigenetic editing in nervous system
Day, J. J. (2019) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2019.21.4/jday · Cited by 13 · see citing works
A multiplexable TALE-based binary expression system for in vivo cellular interaction studies
Tögel, M., Azzam, G., Lee, E. Y., Knapp, D. J. H. F., Tan, Y., Fa, M., & Fulga, T. A. (2017) · Nature Communications · doi:10.1038/s41467-017-01592-3 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Li, C., Brant, E. J., Budak, H., & Zhang, B. (2021) · Journal of Zhejiang University SCIENCE B · doi:10.1631/jzus.b2100009 · Cited by 188 · see citing works
Nectow, A. R., & Nestler, E. J. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-00382-z · Cited by 159 · see citing works
Self-citationKey transcription factors mediating cocaine-induced plasticity in the nucleus accumbens
Teague, C. D., & Nestler, E. J. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01163-5 · Cited by 80 · see citing works
Self-citationPresent and future challenges for the investigation of transgenerational epigenetic inheritance
Fallet, M., Blanc, M., Criscio, M. D., Antczak, P., Engwall, M., Guerrero‐Bosagna, C., Rüegg, J., & Keiter, S. H. (2023) · Environment International · doi:10.1016/j.envint.2023.107776 · Cited by 83 · see citing works
Zheng, X., Wu, B., Liu, Y., Simmons, S., Kim, K., Clarke, G. S., Ashiq, A., Park, J. C., Li, J., Wang, Z., et al. (2024) · Cell · doi:10.1016/j.cell.2024.04.050 · Cited by 80 · see citing works
Cell-type-specific epigenetic effects of early life stress on the brain
Rahman, M. F., & McGowan, P. O. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02076-9 · Cited by 75 · see citing works
Bohnsack, J. P., Zhang, H., Wandling, G. M., He, D., Kyzar, E. J., Lasek, A. W., & Pandey, S. C. (2022) · Science Advances · doi:10.1126/sciadv.abn2748 · Cited by 68 · see citing works
Wang, K., Escobar, M., Li, J., Mahata, B., Goell, J., Shah, S. T., Cluck, M., & Hilton, I. B. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac582 · Cited by 60 · see citing works
Helicobacter pylori-induced NF-κB: trailblazer for gastric pathophysiology
Maubach, G., Vieth, M. W., Boccellato, F., & Naumann, M. (2022) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2021.12.005 · Cited by 57 · 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
D’Incal, C. P., Rossem, K. E. V., Man, K. D., Konings, A., Dijck, A. V., Rizzuti, L., Vitriolo, A., Testa, G., Gozes, I., Berghe, W. V., et al. (2023) · Clinical Epigenetics · doi:10.1186/s13148-023-01450-8 · Cited by 51 · see citing works
From Circuits to Chromatin: The Emerging Role of Epigenetics in Mental Health
Mews, P., Calipari, E. S., Day, J. J., Lobo, M. K., Bredy, T. W., & Abel, T. G. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1649-20.2020 · Cited by 42 · see citing works
Metals Exposures and DNA Methylation: Current Evidence and Future Directions
Elkin, E. R., Tejera, C. H., Aung, M. T., & Bakulski, K. M. (2022) · Current Environmental Health Reports · doi:10.1007/s40572-022-00382-4 · Cited by 44 · see citing works
Campos, L., Arokiaraj, C. M., Chuapoco, M. R., Chen, X., Goeden, N., Gradinaru, V., & Fox, A. S. (2023) · Current Research in Neurobiology · doi:10.1016/j.crneur.2023.100086 · Cited by 41 · see citing works
ΔFOSB: A Potentially Druggable Master Orchestrator of Activity-Dependent Gene Expression
Robison, A. J., & Nestler, E. J. (2022) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.1c00723 · Cited by 42 · see citing works
Self-citationVignali, V., Hines, P. A., Cruz, A. G., Ziętek, B., & Herold, R. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.1064003 · Cited by 43 · see citing works
Fitzgerald, E., Parent, C. I., Kee, M. Z. L., & Meaney, M. J. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.635304 · Cited by 39 · see citing works
Selective Xi reactivation and alternative methods to restore MECP2 function in Rett syndrome
Grimm, N.-B., & Lee, J. T. (2022) · Trends in Genetics · doi:10.1016/j.tig.2022.01.007 · Cited by 33 · see citing works
Polycomb‐mediated gene regulation in human brain development and neurodevelopmental disorders
Bölicke, N., & Albert, M. (2022) · Developmental Neurobiology · doi:10.1002/dneu.22876 · Cited by 34 · see citing works
Liu, S., Yuan, X., Su, H., Liu, F., Zhuang, Z., & Chen, Y. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.892368 · Cited by 35 · see citing works
Fuentes-Ramos, M., Alaiz-Noya, M., & Barco, Á. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.06.010 · Cited by 31 · see citing works
de Sá, R. V., Luna, M. C., & Pasterkamp, R. J. (2021) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2020.0337 · Cited by 30 · see citing works
Application of CRISPR/Cas9 in Rapeseed for Gene Function Research and Genetic Improvement
Tian, Q. C., Li, B., Feng, Y., Zhao, W., Huang, J., & Chao, H. (2022) · Agronomy · doi:10.3390/agronomy12040824 · Cited by 29 · see citing works
Lardner, C. K., van der Zee, Y. Y., Estill, M. S., Kronman, H. G., Salery, M., Cunningham, A. M., Godino, A., Parise, E. M., Kim, J. H., Neve, R. L., et al. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.06.017 · Cited by 28 · see citing works
Self-citationEarly Life Stress- and Drug-Induced Histone Modifications Within the Ventral Tegmental Area
Shepard, R. D., & Nugent, F. S. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.588476 · Cited by 24 · see citing works
Epigenetic mechanisms of nicotine dependence
Muenstermann, C., & Clemens, K. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105505 · Cited by 24 · see citing works
The molecular basis of depression: implications of sex-related differences in epigenetic regulation
Kawatake-Kuno, A., Murai, T., & Uchida, S. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.708004 · Cited by 23 · see citing works
Gene Editing and Modulation: the Holy Grail for the Genetic Epilepsies?
Carpenter, J. C., & Lignani, G. (2021) · Neurotherapeutics · doi:10.1007/s13311-021-01081-y · Cited by 22 · see citing works
Neurobiology of resilience to early life stress
Torres‐Berrío, A., Bortolami, A., Peña, C. J., & Nestler, E. J. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-025-02158-4 · Cited by 24 · see citing works
Self-citationStrategies for Targeting Neural Circuits: How to Manipulate Neurons Using Virus Vehicles
Hui, Y., Zheng, X.-F., Zhang, H., Li, F., Yu, G.-Y., Li, J., Zhang, J.-F., Gong, X.-B., & Guo, G.-Q. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.882366 · Cited by 20 · see citing works
Altered hypothalamic DNA methylation and stress-induced hyperactivity following early life stress
Fitzgerald, E., Sinton, M. C., Wernig-Zorc, S., Morton, N. M., Holmes, M. C., Boardman, J. P., & Drake, A. J. (2021) · Epigenetics & Chromatin · doi:10.1186/s13072-021-00405-8 · Cited by 19 · see citing works
Teague, C. D., Picone, J. A., Wright, W. J., Browne, C. J., Silva, G. M., Futamura, R., Minier-Toribio, A. M., Estill, M. S., Ramakrishnan, A., Martínez-Rivera, F. J., et al. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.07.022 · Cited by 18 · see citing works
Self-citationCentral and peripheral stress-induced epigenetic mechanisms of resilience
Dudek, K., Kaufmann, F. N., Lavoie, O., & Ménard, C. (2020) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000664 · Cited by 18 · see citing works
PIWI-Interacting RNA (piRNA) and Epigenetic Editing in Environmental Health Sciences
Perera, B. P. U., Morgan, R. K., Polemi, K. M., Sala-Hamrick, K. E., Svoboda, L. K., & Dolinoy, D. C. (2022) · Current Environmental Health Reports · doi:10.1007/s40572-022-00372-6 · Cited by 17 · see citing works
Alkhammash, A., & Alotaibi, G. (2025) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2025.177853 · Cited by 15 · see citing works
DNA methylation-environment interactions in the human genome
Johnston, R. A., Aracena, K. A., Barreiro, L. B., Lea, A. J., & Tung, J. (2024) · eLife · doi:10.7554/elife.89371.3 · Cited by 14 · see citing works
Imbriano, C., & Belluti, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158304 · Cited by 13 · see citing works
Gong, L., Liu, X., Wu, J., & He, M. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01292-x · Cited by 8 · see citing works
Neuronal Cell-type Engineering by Transcriptional Activation
Liu, S., Striebel, J., Pasquini, G., Ng, A. H. M., Khoshakhlagh, P., Church, G. M., & Busskamp, V. (2021) · Frontiers in Genome Editing · doi:10.3389/fgeed.2021.715697 · Cited by 11 · see citing works
Neurogenesis and Neuroinflammation in Dialogue: Mapping Gaps, Modulating Microglia, Rewiring Aging
Tanaka, M. (2026) · Cells · doi:10.3390/cells15010078 · Cited by 11 · see citing works
Marei, H. E. S. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-05590-1 · Cited by 11 · see citing works
Singh, S. M., Castellani, C. A., & Hill, K. A. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.587162 · Cited by 11 · see citing works
Regulation of NR4A2 Gene Expression and Its Importance in Neurodegenerative and Psychiatric Diseases
Ruiz-Sánchez, E., Rojas, C., Gómez, P. Y., Martínez‐Rodríguez, N., Ruíz-Chow, Á. A., Nava-Ruíz, C., Ibáñez-Cervantes, G., Arciniega-Martínez, I. M., Reséndiz‐Albor, A. A., & Rojas, P. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26189162 · Cited by 9 · see citing works
DNA methylation-environment interactions in the human genome
Johnston, R. A., Aracena, K. A., Barreiro, L. B., Lea, A. J., & Tung, J. (2023) · eLife · doi:10.7554/elife.89371 · Cited by 8 · see citing works
Saeliw, T., Kanlayaprasit, S., Thongkorn, S., Songsritaya, K., Sanannam, B., Jindatip, D., Hu, V. W., & Sarachana, T. (2024) · Scientific Reports · doi:10.1038/s41598-024-72334-x · Cited by 8 · see citing works
Psychiatric Genetics in Clinical Practice: Essential Knowledge for Mental Health Professionals
Besterman, A. D., Alnor, M. A., Castaño, M., DeLisi, L. E., Grice, D. E., Lohoff, F. W., Middeldorp, C. M., Müller, D. J., Quattrone, D., Nürnberger, J. I., et al. (2025) · American Journal of Psychiatry · doi:10.1176/appi.ajp.20240295 · Cited by 8 · see citing works
Sourty, M., Nasseef, M. T., Liberti, C. C.-D., Mondino, M., Noblet, V., Parise, E. M., Markovic, T., Browne, C. J., Darcq, E., Nestler, E. J., et al. (2023) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.07.013 · Cited by 6 · see citing works
Self-citationMolecular and cellular mechanisms of engram allocation and maintenance
Karaca, K. G., Kupke, J., & Oliveira, A. M. M. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.02.019 · Cited by 7 · see citing works
Get ready for the CRISPR/Cas system: A beginner's guide to the engineering and design of guide RNAs
Ma, S., Lv, J., Feng, Z., Rong, Z., & Lin, Y. (2021) · The Journal of Gene Medicine · doi:10.1002/jgm.3377 · Cited by 6 · see citing works
Application of novel CRISPR tools in brain therapy
Shang, J., Song, F., Zhang, Z., Chen, D., & Yang, S. (2024) · Life Sciences · doi:10.1016/j.lfs.2024.122855 · Cited by 5 · see citing works
Teenage drinking and adult neuropsychiatric disorders: An epigenetic connection
Teague, C. D., & Nestler, E. J. (2022) · Science Advances · doi:10.1126/sciadv.abq5934 · Cited by 5 · see citing works
Self-citationUncovering methylation-dependent genetic effects on regulatory element function in diverse genomesPreprint
Petersen, R. M., Vockley, C. M., & Lea, A. J. (2025) · Genome Research · doi:10.1101/gr.279957.124 · Cited by 4 · see citing works
Fernández, G. R., Leiva, K., Bustos, F. J., & van Zundert, B. (2025) · Clinical Epigenetics · doi:10.1186/s13148-025-01903-2 · Cited by 3 · see citing works
Akyürek, E., Uysal, B., Gülden, G., & Taştan, C. (2021) · Gene Editing · doi:10.29228/genediting.54941 · Cited by 2 · see citing works
Advances in approaches to study cell-type specific cortical circuits throughout development
Hanson, M. A., & Wester, J. C. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.1031389 · Cited by 2 · see citing works
CUT&RUN as a Powerful Tool for Chromatin Profiling: A Focus on Neuropsychiatric Disorders
Holt, L. M., Chen, E. P., Hughes, B. W., & Nestler, E. J. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2025.08.012 · Cited by 1 · see citing works
Self-citationParadigms for establishing long-term epigenetic states in brain
O’Geen, H., & Segal, D. J. (2026) · Current Opinion in Biomedical Engineering · doi:10.1016/j.cobme.2026.100665 · Cited by 1 · see citing works
Shepard, R. D., & Nugent, F. S. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-91909-8.00040-2 · Cited by 1 · see citing works
Epigenetic Priming of Activity-Dependent Transcription in Drug Addiction
Hughes, B. W., & Nestler, E. J. (2024) · Springer eBooks · doi:10.1007/978-3-031-68550-7_13 · Cited by 1 · see citing works
Self-citationDNA methylation-environment interactions in the human genomePreprint
Johnston, R. A., Aracena, K. A., Barreiro, L. B., Lea, A. J., & Tung, J. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.19.541437 · Cited by 1 · see citing works
Sokpor, G., Ulmke, P. A., Nguyen, H. D., Pham, L., Kakani, P., Chu, V. T., Arnold, S. J., Brand‐Saberi, B., Nguyen, H. P., & Tuoc, T. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.05.621758 · Cited by 1 · see citing works
Nguyen, J., Byragoni, N., Arinzeh, N., Bortolami, A., Sidoli, S., Russo, S. J., Nestler, E. J., & Torres‐Berrío, A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.25.690167 · Cited by 1 · see citing works
Self-citationAlomrani, B., Javed, M., Ali, H. S. H. M., Abo‐Aba, S. E. M., AlBakheet, A., AlQudairy, H., & Kaya, N. (2022) · Journal of Contemporary Medical Sciences · doi:10.22317/jcms.v8i1.1167
DNA methylation-environment interactions in the human genomePreprint
Johnston, R. A., Aracena, K. A., Barreiro, L. B., Lea, A. J., & Tung, J. (2023) · eLife · doi:10.7554/elife.89371.1
DNA methylation-environment interactions in the human genomePreprint
Johnston, R. A., Aracena, K. A., Barreiro, L. B., Lea, A. J., & Tung, J. (2024) · eLife · doi:10.7554/elife.89371.2
Persistent in vivo epigenetic silencing of Pcsk9
Gengaro, I. R., & Qi, L. S. (2024) · Cell Research · doi:10.1038/s41422-024-00954-z
Uncovering methylation-dependent genetic effects on regulatory element function in diverse genomesPreprint
Petersen, R. M., Vockley, C. M., & Lea, A. J. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.08.23.609412
Environmental molecular physiology
(2023) · CSIRO Publishing eBooks · doi:10.1071/9781486314935.bk08025_part4
Fitzgerald, E., Sinton, M. C., Wernig-Zorc, S., Morton, N. M., Holmes, M. C., Boardman, J. P., & Drake, A. J. (2021) · Figshare · doi:10.6084/m9.figshare.14889222
Kalomoiri, M., Sorini, C., Vos, S. V. T., Camargo, A., Tsalikou, A., Krstic, A., Prakash, C. R., Svenningsson, P., Needhamsen, M., Kakhki, M. P., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.26.708277
The human brain: Medicine's last frontier.
Nestler, E. J. (2026) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2026.103189
Self-citationRenewal and reacquisition of substance-associated relapse
Rodríguez‐Lausell, I., Goold, T. M., Fileni, R. G., Aggarwal-Matto, R., & Martínez-Rivera, F. J. (2026) · Frontiers in Psychology · doi:10.3389/fpsyg.2026.1781712
Sokpor, G., Ulmke, P. A., Nguyen, H. D., Pham, L., Kakani, P., Chu, V. T., Arnold, S. J., Brand‐Saberi, B., Nguyen, H. P., & Tuoc, T. (2026) · Biology · doi:10.3390/biology15141110
Recent Advances in CRISPR/Cas Technologies for Biological Discovery, Therapeutics, and Diagnostics
Kim, M., Do, H. S., Jang, H. Y., Lee, K. E., & Lee, S. J. (2026) · Biomolecules · doi:10.3390/biom16091268
Epigenetic mechanisms in stress and the hypothalamic-pituitary-adrenal axis
WEAVER, I. C. G. (2026) · Handbook of clinical neurology · doi:10.1016/b978-0-443-19043-8.00018-9
- Authors
- Yim, Y. Y., Teague, C. D., & Nestler, E. J.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- Corresponding author
- Nestler, Eric J.
- Venue
- Nature Reviews Neuroscience
- Published
- 2020-07-23
- Volume
- 21
- Issue
- 9
- Pages
- 471-484
- ISSN
- 1471-003X (ISSN-L)
- 1471-0048
- PMC
- PMC7439525
- OpenAlex
- W3044612680
- Cited by
- 76
- References
- 110
- Citations by year
- 2026: 8 · 2025: 9 · 2024: 11 · 2023: 9 · 2022: 19 · 2021: 16 · 2020: 4
- FWCI
- 1.15
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature reviews. Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH051399)
- National Institute on Drug Abuse (P01DA047233, R01DA007359)
- 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 › Genomics and Chromatin Dynamics
- Keywords
- chromatin modification, zinc finger proteins, CRISPR, chromatin topology
- MeSH terms
- Gene Editing, Animals, Brain Diseases, Chromatin, Humans, Epigenesis, Genetic, Epigenomics
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