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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Differential splicing events in ASD cortex are significantly enriched in events previously shown to be regulated by neuronal activity.
“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]
Covalent modifications of DNA and some histone proteins in post-mitotic neurons can persist for months to years.
“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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- 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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