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Critical Role of Histone Turnover in Neuronal Transcription and Plasticity
Open accessAbstract
Turnover and exchange of nucleosomal histones and their variants, a process long believed to be static in post-replicative cells, remains largely unexplored in brain. Here, we describe a novel mechanistic role for HIRA (histone cell cycle regulator) and proteasomal degradation-associated histone dynamics in the regulation of activity-dependent transcription, synaptic connectivity, and behavior. We uncover a dramatic developmental profile of nucleosome occupancy across the lifespan of both rodents and humans, with the histone variant H3.3 accumulating to near-saturating levels throughout the neuronal genome by mid-adolescence. Despite such accumulation, H3.3-containing nucleosomes remain highly dynamic-in a modification-independent manner-to control neuronal- and glial-specific gene expression patterns throughout life. Manipulating H3.3 dynamics in both embryonic and adult neurons confirmed its essential role in neuronal plasticity and cognition. Our findings establish histone turnover as a critical and previously undocumented regulator of cell type-specific transcription and plasticity in mammalian brain.
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“Indeed, differential splicing events were significantly enriched in those previously shown to be regulated by neuronal activity21 (Fig. 1h).”
From Genome-wide changes in lncRNA, splicing, and regional gene expression patterns in autism (2016) · cites this paper as [21]
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“covalent modifications of DNA and some histone proteins in post-mitotic neurons can persist for months to years (Maze et al., 2015).”
From Single-Cell Sequencing of Brain Cell Transcriptomes and Epigenomes (2021) · cites this paper as Maze et al., 2015
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Metadata
- Authors
- Maze, I., Wenderski, W., Noh, K.-M., Bagot, R. C., Tzavaras, N., Purushothaman, I., Elsässer, S. J., Guo, Y., Ionete, C., Hurd, Y. L., Tamminga, C. A., Halene, T., Farrelly, L., Soshnev, A. A., Wen, D., Rafii, S., Birtwistle, M. R., Akbarian, S., Buchholz, B. A., Blitzer, R. D., Nestler, E. J., Yuan, Z.-F., Garcia, B. A., Shen, L., Molina, H., & Allis, C. D.
- Affiliations
- Rockefeller University (US)
- Icahn School of Medicine at Mount Sinai (US)
- UMass Memorial Medical Center (US)
- The University of Texas Southwestern Medical Center (US)
- Weill Cornell Medicine (US)
- Lawrence Livermore National Laboratory (US)
- University of Pennsylvania (US)
- Corresponding author
- Maze, Ian
- Allis, C. David
- ORCID
- Maze, Ian
- Noh, Kyung-Min
- Bagot, Rosemary C.
- Tzavaras, Nikos
- Elsässer, Simon J.
- Guo, Yin
- Ionete, Carolina
- Hurd, Yasmin L.
- Tamminga, Carol A.
- Halene, Tobias
- Farrelly, Lorna
- Soshnev, Alexey A.
- Wen, Duancheng
- Rafii, Shahin
- Birtwistle, Marc R.
- Akbarian, Schahram
- Buchholz, Bruce A.
- Blitzer, Robert D.
- Nestler, Eric J.
- Yuan, Zuo-Fei
- Garcia, Benjamin A.
- Shen, Li
- Molina, Henrik
- Allis, C. David
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2015-07
- Volume
- 87
- Issue
- 1
- Pages
- 77-94
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC4491146
- OpenAlex
- W1579352208
- Cited by
- 306
- References
- 23
- Citations by year
- 2026: 21 · 2025: 20 · 2024: 23 · 2023: 36 · 2022: 29 · 2021: 21 · 2020: 38 · 2019: 24 · 2018: 31 · 2017: 26 · 2016: 28 · 2015: 8
- FWCI
- 13.45
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 366 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- Funders
- National Institute of Mental Health (5R01 MH094698, P50 MH096890)
- NIH (R21MH102679, RO1GM110174, 8P41GM103483)
- US Department of Energy by Lawrence Livermore National Laboratory (DE-AC52-07NA27344, LLNL-JRNL-653296)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- histone turnover, histone H3.3, histone variants, synaptic plasticity, nucleosome occupancy, HIRA, proteasomal degradation, activity-dependent gene expression, cognitive function, brain development, cell type-specific gene expression
- MeSH terms
- Adolescent, Adult, Aged, Animals, Brain, Cerebellum, Child, Child, Preschool, Chromatin, Female, Fetus, Frontal Lobe, Hippocampus, Histones, Humans, Male, Middle Aged, Neuronal Plasticity, Neurons, Nucleosomes, Transcription, Genetic, Gene Expression Regulation, Developmental, Epigenesis, Genetic, Mice, Young Adult
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