HDAC3 Is a Critical Negative Regulator of Long-Term Memory Formation
Open accessAbstract
Gene expression is dynamically regulated by chromatin modifications on histone tails, such as acetylation. In general, histone acetylation promotes transcription, whereas histone deacetylation negatively regulates transcription. The interplay between histone acetyltranserases and histone deacetylases (HDACs) is pivotal for the regulation of gene expression required for long-term memory processes. Currently, very little is known about the role of individual HDACs in learning and memory. We examined the role of HDAC3 in long-term memory using a combined genetic and pharmacologic approach. We used HDAC3–FLOX genetically modified mice in combination with adeno-associated virus-expressing Cre recombinase to generate focal homozygous deletions of Hdac3 in area CA1 of the dorsal hippocampus. To complement this approach, we also used a selective inhibitor of HDAC3, RGFP136 [ N -(6-(2-amino-4-fluorophenylamino)-6-oxohexyl)-4-methylbenzamide]. Immunohistochemistry showed that focal deletion or intrahippocampal delivery of RGFP136 resulted in increased histone acetylation. Both the focal deletion of HDAC3 as well as HDAC3 inhibition via RGFP136 significantly enhanced long-term memory in a persistent manner. Next we examined expression of genes implicated in long-term memory from dorsal hippocampal punches using quantitative reverse transcription-PCR. Expression of nuclear receptor subfamily 4 group A, member 2 ( Nr4a2 ) and c-fos was significantly increased in the hippocampus of HDAC3–FLOX mice compared with wild-type controls. Memory enhancements observed in HDAC3–FLOX mice were abolished by intrahippocampal delivery of Nr4a2 small interfering RNA, suggesting a mechanism by which HDAC3 negatively regulates memory formation. Together, these findings demonstrate a critical role for HDAC3 in the molecular mechanisms underlying long-term memory formation.
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Dorsal CA1 is a region crucial for normal memory function.
“a region crucial to normal memory function,25”
From Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress (2014) · cites this paper as [25]
Dorsal hippocampus, and in particular CA1, has a greater role in memory functions.
“these data are in line with the greater role of memory functions subserved by dorsal hippocampus, and in particular by CA1 region25,75”
From Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress (2014) · cites this paper as [25]
Dorsal hippocampus in the rodent, primarily CA1, is the principal location of memory encoding and processing.
“Dorsal hippocampus in the rodent, and primarily CA1, has emerged as the principal location of memory encoding and processing”
From Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress (2014) · cites this paper as [25]
Ventral hippocampus contributes to a network involved in salience and emotionality.
“ventral hippocampus contributes to a network involved in salience and emotionality.9,10,25,117”
From Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress (2014) · cites this paper as [25]
HDAC3-flox mice injected with AAV-Cre recombinase into the hippocampal CA1 region to selectively deplete HDAC3 in CA1 showed enhanced long-term OPP memory.
“HDAC3-flox mice injected with AAV-Cre recombinase into the hippocampal CA1 region to selectively deplete HDAC3 in CA1, showed enhanced long-term OPP memory.”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as McQuown et al., 2011
Similar results were found in mice with intra-CA1 infusions of RGFP136, a selective HDAC3 inhibitor.
“Similar results were found in mice with the intra-CA1 infusions of RGFP136, a selective HDAC3 inhibitor”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as McQuown et al., 2011
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- Authors
- McQuown, S. C., Barrett, R. M., Matheos, D. P., Post, R. J., Rogge, G. A., Alenghat, T., Mullican, S. E., Jones, S., Rusche, J. R., Lazar, M. A., & Wood, M. A.
- Affiliations
- University of California, Irvine (US)
- University of Pennsylvania (US)
- Repligen (United States) (US)
- Corresponding author
- Wood, Marcelo A.
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-01-12
- Volume
- 31
- Issue
- 2
- Pages
- 764-774
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3160172
- OpenAlex
- W1976507388
- Cited by
- 507
- References
- 44
- Citations by year
- 2026: 17 · 2025: 21 · 2024: 28 · 2023: 25 · 2022: 18 · 2021: 32 · 2020: 31 · 2019: 34 · 2018: 34 · 2017: 31 · 2016: 42 · 2015: 28 · 2014: 59 · 2013: 51 · 2012: 31
- FWCI
- 26.79
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Whitehall Foundation
- University of Pennsylvania
- National Institutes of Health (DK 19525, DK43806)
- National Institute of Mental Health (R01MH081004, F31MH085494)
- National Institute on Drug Abuse (R01DA025922)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK43806, R37DK043806, R01DK043806, P30DK019525)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Histone Deacetylase Inhibitors Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- HDAC3, histone deacetylase, long-term memory, memory formation, histone acetylation, chromatin modification, dorsal hippocampus, CA1, Nurr1, c-fos, gene expression regulation, learning and memory
- MeSH terms
- Histone Deacetylase 3, Acetylation, Animals, Benzamides, Hippocampus, Histone Deacetylases, Histones, Mice, Mutant Strains, Space Perception, Sequence Deletion, Mice, Histone Deacetylase Inhibitors, Nuclear Receptor Subfamily 4, Group A, Member 2, Memory, Long-Term
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.
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