A modular dCas9-SunTag DNMT3A epigenome editing system overcomes pervasive off-target activity of direct fusion dCas9-DNMT3A constructs
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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.
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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]
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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
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