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Circadian clock proteins regulate neuronal redox homeostasis and neurodegeneration
Open accessAbstract
Brain aging is associated with diminished circadian clock output and decreased expression of the core clock proteins, which regulate many aspects of cellular biochemistry and metabolism. The genes encoding clock proteins are expressed throughout the brain, though it is unknown whether these proteins modulate brain homeostasis. We observed that deletion of circadian clock transcriptional activators aryl hydrocarbon receptor nuclear translocator-like (Bmal1) alone, or circadian locomotor output cycles kaput (Clock) in combination with neuronal PAS domain protein 2 (Npas2), induced severe age-dependent astrogliosis in the cortex and hippocampus. Mice lacking the clock gene repressors period circadian clock 1 (Per1) and period circadian clock 2 (Per2) had no observed astrogliosis. Bmal1 deletion caused the degeneration of synaptic terminals and impaired cortical functional connectivity, as well as neuronal oxidative damage and impaired expression of several redox defense genes. Targeted deletion of Bmal1 in neurons and glia caused similar neuropathology, despite the retention of intact circadian behavioral and sleep-wake rhythms. Reduction of Bmal1 expression promoted neuronal death in primary cultures and in mice treated with a chemical inducer of oxidative injury and striatal neurodegeneration. Our findings indicate that BMAL1 in a complex with CLOCK or NPAS2 regulates cerebral redox homeostasis and connects impaired clock gene function to neurodegeneration.
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In the citing paper
“In vivo BMAL1 deletion was found to induce activation of glial cells and degeneration of presynaptic axonal terminals.122”
From Role of neuroinflammation in neurodegeneration development (2023) · cites this paper as [122]
In the citing paper
“Circadian rhythms have been shown to regulate redox homeostasis in the brain, and disruption of circadian genes causes neuronal oxidative damage (Musiek et al., 2013).”
From Clock Genes Control Cortical Critical Period Timing (2015) · cites this paper as Musiek et al., 2013
In the citing paper
“mice with a brain-specific Bmal1 deletion also exhibit increased astrocytosis, despite having mostly normal locomotor circadian rhythms and sleep–wake cycling (that is, relatively normal clock function in the SCN); thus, these neurodegenerative effects are probably due to loss of the local control of cellular metabolism in specific regions of the brain that is normally mediated by BMAL1, indep”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [291]
In the citing paper
“ROS accumulation is considerably higher in Bmal1−/− mice and correlates with increases in astrocytosis and levels of oxidative damage markers in the brain.”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [291]
In the citing paper
“Bmal1−/− mice, which lack a functional molecular clock, show premature ageing, neurodegeneration and a reduced lifespan291.”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [291]
In the citing paper
“This preclinical investigation demonstrates that components of the molecular clock control redox state and, when disrupted, lead to oxidative stress and cell death related to neurodegeneration.”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [291]
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Ma, J., Ma, N., Zhang, L., Xu, L., Liu, X., & Meng, G. (2024) · BMC Neurology · doi:10.1186/s12883-024-03727-8 · Cited by 6
Li, P., & Hu, K. (2025) · SLEEP · doi:10.1093/sleep/zsaf047 · Cited by 4
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Long, D. M., Cravetchi, O., Chow, E. S., Allen, C. N., & Kretzschmar, D. (2024) · Neurobiology of Disease · doi:10.1016/j.nbd.2024.106429 · Cited by 5
Human CLOCK enhances neocortical function
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Baba, K., Suen, T.-C., Goyal, V., Stowie, A. C., Davidson, A. J., DeBruyne, J. P., & Tosini, G. (2022) · F1000Research · doi:10.12688/f1000research.125133.1 · Cited by 4
Chrono‐Gerontology: Integrating Circadian Rhythms and Aging in Stroke Research
Kara, N. Z., Iweka, C. A., & Blacher, E. (2023) · Advanced Biology · doi:10.1002/adbi.202300048 · Cited by 5
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Metadata
- Authors
- Musiek, E. S., Lim, M. M., Yang, G., Bauer, A. Q., Qi, L., Lee, Y., Roh, J. H., Ortiz-Gonzalez, X., Dearborn, J. T., Culver, J. P., Herzog, E. D., Hogenesch, J. B., Wozniak, D. F., Dikranian, K., Giasson, B. I., Weaver, D. R., Holtzman, D. M., & FitzGerald, G. A.
- Affiliations
- Washington University in St. Louis (US)
- University of Pennsylvania (US)
- University of Florida (US)
- University of Massachusetts Chan Medical School (US)
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2013-11-25
- Volume
- 123
- Issue
- 12
- Pages
- 5389-5400
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC3859381
- OpenAlex
- W2003062381
- Cited by
- 524
- References
- 59
- Citations by year
- 2026: 35 · 2025: 54 · 2024: 46 · 2023: 58 · 2022: 53 · 2021: 48 · 2020: 47 · 2019: 34 · 2018: 42 · 2017: 29 · 2016: 30 · 2015: 23 · 2014: 23 · 2013: 2
- FWCI
- 14.04
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Commons@Becker (Washington University School of Medicine) (submittedVersion)
- eScholarship@UMassChan (submittedVersion, other-oa)
- Funders
- Ellison Medical Foundation
- Cure Alzheimer's Fund (P01NS074969)
- Hope Center for Neurological Disorders (P30 NS057105)
- National Institutes of Health (HL097800, NS057105)
- National Institute on Aging (P50AG005681)
- National Heart, Lung, and Blood Institute (HL 097800, R01HL097800)
- National Institute of Neurological Disorders and Stroke (NS-056125, P30NS057105, R01NS078223, K08NS079405, R25NS065745, R01NS056125, P01NS074969)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- circadian clock proteins, Bmal1, clocks, NPAS2, Per1, Per2, redox homeostasis, oxidative stress, neurodegeneration, brain aging, astrocyte activation, synaptic degeneration, cortical functional connectivity, neuronal cell death, striatal degeneration
- MeSH terms
- Aging, Animals, Brain, Cerebral Cortex, Circadian Rhythm, Corpus Striatum, Gene Expression Regulation, Gliosis, Hippocampus, Homeostasis, Locomotion, Mice, Inbred C57BL, Mice, Neurologic Mutants, Nerve Degeneration, Nerve Tissue Proteins, Neuroglia, Neurons, Oxidation-Reduction, Mice, Knockout, Oxidative Stress, Sleep Disorders, Circadian Rhythm, RNA Interference, Basic Helix-Loop-Helix Transcription Factors, Basic Helix-Loop-Helix Proteins, CLOCK Proteins, ARNTL Transcription Factors, Period Circadian Proteins
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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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