A NPAS4–NuA4 complex couples synaptic activity to DNA repair
Open accessAbstract
Neuronal activity is crucial for adaptive circuit remodelling but poses an inherent risk to the stability of the genome across the long lifespan of postmitotic neurons 1–5. Whether neurons have acquired specialized genome protection mechanisms that enable them to withstand decades of potentially damaging stimuli during periods of heightened activity is unknown. Here we identify an activity-dependent DNA repair mechanism in which a new form of the NuA4–TIP60 chromatin modifier assembles in activated neurons around the inducible, neuronal-specific transcription factor NPAS4. We purify this complex from the brain and demonstrate its functions in eliciting activity-dependent changes to neuronal transcriptomes and circuitry. By characterizing the landscape of activity-induced DNA double-strand breaks in the brain, we show that NPAS4–NuA4 binds to recurrently damaged regulatory elements and recruits additional DNA repair machinery to stimulate their repair. Gene regulatory elements bound by NPAS4–NuA4 are partially protected against age-dependent accumulation of somatic mutations. Impaired NPAS4–NuA4 signalling leads to a cascade of cellular defects, including dysregulated activity-dependent transcriptional responses, loss of control over neuronal inhibition and genome instability, which all culminate to reduce organismal lifespan. In addition, mutations in several components of the NuA4 complex are reported to lead to neurodevelopmental and autism spectrum disorders. Together, these findings identify a neuronal-specific complex that couples neuronal activity directly to genome preservation, the disruption of which may contribute to developmental disorders, neurodegeneration and ageing.
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NPAS4 is a TF that protects against age-dependent accumulation of DNA damages and somatic mutations.
“NPAS4, a TF that protects against age-dependent accumulation of DNA damages and somatic mutations (76)”
From Modeling late-onset Alzheimer’s disease neuropathology via direct neuronal reprogramming (2024) · cites this paper as [76]
The ‘Age-dependent mutations at NPAS4 sites’ section reports that NPAS4–NuA4-bound sites in mouse hippocampal neurons were relatively protected from mutations accumulating with age. The ‘NPAS4–NuA4 disruption impairs DSB repair’ section also reports more DNA double-strand breaks after NPAS4 deletion. The claim is broader than these findings: the mutation result concerns specific bound sites, and the paper does not establish protection against age-dependent accumulation of DNA damage generally. (LLM, conf=0.86)
Experimental — accuracy not yet measuredSome of the downregulated genes were NPAS4 and PIWIL2.
“Some of the downregulated genes were NPAS4, a TF that protects against age-dependent accumulation of DNA damages and somatic mutations (76), and PIWIL2, one of the four known human Piwi proteins (Fig. 6A and Fig. S11B).”
From Modeling late-onset Alzheimer’s disease neuropathology via direct neuronal reprogramming (2024) · cites this paper as [76]
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- Authors
- Pollina, E. A., Gilliam, D. T., Landau, A. T., Lin, C., Pajarillo, N., Davis, C. P., Harmin, D. A., Yap, E.-L., Vogel, I. R., Griffith, E. C., Nagy, M. A., Ling, E., Duffy, E. E., Sabatini, B. L., Weitz, C. J., & Greenberg, M. E.
- Affiliations
- Harvard University (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Greenberg, Michael E.
- ORCID
- Venue
- Nature
- Published
- 2023-02-15
- Volume
- 614
- Issue
- 7949
- Pages
- 732-741
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC9946837
- OpenAlex
- W4320913125
- Cited by
- 125
- References
- 74
- Citations by year
- 2026: 26 · 2025: 40 · 2024: 34 · 2023: 25
- FWCI
- 11.14
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Nature (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Paul G. Allen Family Foundation
- Damon Runyon Cancer Research Foundation
- Good Ventures Foundation
- National Institutes of Health (NS007473, NS072030, NS028829)
- National Institute on Aging (K99AG064042)
- National Institute of General Medical Sciences (T32GM007753)
- National Institute of Neurological Disorders and Stroke (NS007473, F32NS112455, #NS072030, P30NS072030, R01NS028829, R37NS046579, T32NS007473)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P50HD105351)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- Npas4, NuA4 complex, Tip60, chromatin modifiers, DNA double-strand breaks, synaptic activity, genome stability, neuronal transcriptome, somatic mutations, lifespan, neuronal inhibition, autism spectrum disorder, neurodevelopmental disorders, neurodegeneration, aging
- MeSH terms
- Lysine Acetyltransferase 5, Aging, Brain, DNA Repair, Gene Expression Regulation, Longevity, Mutation, Neurons, Synapses, Genome, Neurodegenerative Diseases, Multiprotein Complexes, Basic Helix-Loop-Helix Transcription Factors, Basic Helix-Loop-Helix Proteins, DNA Breaks, Double-Stranded
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