A role for clock genes in sleep homeostasis

Franken, Paul

doi:10.1016/j.conb.2013.05.002

Cited by 125Circadian rhythm and melatoninSleep and Wakefulness ResearchSleep and Work-Related Fatigue

A role for clock genes in sleep homeostasis

Franken, Paul·2013·Current Opinion in Neurobiology

DOI 10.1016/j.conb.2013.05.002

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Abstract

The timing and quality of both sleep and wakefulness are thought to be regulated by the interaction of two processes. One of these two processes keeps track of the prior sleep-wake history and controls the homeostatic need for sleep while the other sets the time-of-day that sleep preferably occurs. The molecular pathways underlying the latter, circadian process have been studied in detail and their key role in physiological time-keeping has been well established. Analyses of sleep in mice and flies lacking core circadian clock gene proteins have demonstrated, however, that besides disrupting circadian rhythms, also sleep homeostatic processes were affected. Subsequent studies revealed that sleep loss alters both the mRNA levels and the specific DNA-binding of the key circadian transcriptional regulators to their target sequences in the mouse brain. The fact that sleep loss impinges on the very core of the molecular circadian circuitry might explain why both inadequate sleep and disrupted circadian rhythms can similarly lead to metabolic pathology. The evidence for a role for clock genes in sleep homeostasis will be reviewed here.

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Sleep is an emergent set of many physiologic processes under primarily neurobiological regulation that impact many physiologic systems.
“Sleep represents an emergent set of many physiologic processes under primarily neurobiological regulation that impact many physiologic systems.”
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The two‐process model of sleep regulation: a reappraisal
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Sleep, Health, and Society
Grandner, M. A. (2020) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2020.02.017 · Cited by 139 · see citing works
Galanin Neurons Unite Sleep Homeostasis and α2-Adrenergic Sedation
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Gating and the Need for Sleep: Dissociable Effects of Adenosine A1 and A2A Receptors
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Phenotyping of PER3 variants reveals widespread effects on circadian preference, sleep regulation, and health
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Sleep–wake-driven and circadian contributions to daily rhythms in gene expression and chromatin accessibility in the murine cortex
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Circadian Factor BMAL1 in Histaminergic Neurons Regulates Sleep Architecture
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Motor-Activity Markers of Circadian Timekeeping Are Related to Ketamine’s Rapid Antidepressant Properties
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Sleep in Normal Aging, Homeostatic and Circadian Regulation and Vulnerability to Sleep Deprivation
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Shank3 modulates sleep and expression of circadian transcription factors
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Cold-inducible RNA-binding protein (CIRBP) adjusts clock-gene expression and REM-sleep recovery following sleep deprivation
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Deletion of theSnord116/SNORD116Alters Sleep in Mice and Patients with Prader-Willi Syndrome
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Circadian rhythms and attention deficit hyperactivity disorder: The what, the when and the why
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The circadian clock at the intercept of sleep and pain
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In Vivo Imaging of the Central and Peripheral Effects of Sleep Deprivation and Suprachiasmatic Nuclei Lesion on PERIOD-2 Protein in Mice
Curie, T., Maret, S., Emmenegger, Y., & Franken, P. (2015) · SLEEP · doi:10.5665/sleep.4974 · Cited by 67 · see citing works
Dysfunction of ventral tegmental area GABA neurons causes mania-like behavior
Yu, X., Ba, W., Zhao, G., Ma, Y., Harding, E. C., Yin, L., Wang, D., Li, H., Zhang, P., Shi, Y., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0810-9 · Cited by 64 · see citing works
Ketamine-Induced Glutamatergic Mechanisms of Sleep and Wakefulness: Insights for Developing Novel Treatments for Disturbed Sleep and Mood
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Altered Sleep Homeostasis inRev-erbα Knockout Mice
Mang, G. M., Spada, F. L., Emmenegger, Y., Chappuis, S., Ripperger, J. A., Albrecht, U., & Franken, P. (2016) · SLEEP · doi:10.5665/sleep.5534 · Cited by 60 · see citing works
Clock Genes and Light Signaling Alterations in Bipolar Disorder: When the Biological Clock Is Off
Geoffroy, P. A. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.09.006 · Cited by 60 · see citing works
Sleep-Wake Regulation and Its Impact on Working Memory Performance: The Role of Adenosine
Reichert, C., Maire, M., Schmidt, C., & Cajochen, C. (2016) · Biology · doi:10.3390/biology5010011 · Cited by 56 · see citing works
Single-cell transcriptomics reveals that glial cells integrate homeostatic and circadian processes to drive sleep–wake cycles
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Polymorphisms in the circadian expressed genes PER3 and ARNTL2 are associated with diurnal preference and GNβ3 with sleep measures
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Cross‐talk between circadian clocks, sleep‐wake cycles, and metabolic networks: Dispelling the darkness
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An essential role for MEF2C in the cortical response to loss of sleep in mice
Bjorness, T. E., Kulkarni, A., Rybalchenko, V., Suzuki, A., Bridges, C., Harrington, A. J., Cowan, C. W., Takahashi, J. S., Konopka, G., & Greene, R. W. (2020) · eLife · doi:10.7554/elife.58331 · Cited by 50 · see citing works
NMDA Receptors in the Lateral Preoptic Hypothalamus Are Essential for Sustaining NREM and REM Sleep
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Necdin regulates BMAL1 stability and circadian clock through SGT1-HSP90 chaperone machinery
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Chronic Fragmentation of the Daily Sleep-Wake Rhythm Increases Amyloid-beta Levels and Neuroinflammation in the 3xTg-AD Mouse Model of Alzheimer’s Disease
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The Zfhx3-Mediated Axis Regulates Sleep and Interval Timing in Mice
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Mutual influence of sleep and circadian clocks on physiology and cognition
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Genetic Dissection of Sleep Homeostasis
Mang, G. M., & Franken, P. (2013) · Current topics in behavioral neurosciences · doi:10.1007/7854_2013_270 · Cited by 35 · see citing works
Sustained Sleep Fragmentation Induces Sleep Homeostasis in Mice
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Sleep homeostasis during daytime food entrainment in mice
Northeast, R. C., Huang, Y., McKillop, L. E., Bechtold, D. A., Peirson, S. N., Piggins, H. D., & Vyazovskiy, V. V. (2019) · SLEEP · doi:10.1093/sleep/zsz157 · Cited by 32 · see citing works
Propofol improves sleep deprivation‐induced sleep structural and cognitive deficits via upregulating the BMAL1 expression and suppressing microglial M1 polarization
Liu, H., Yang, C., Wang, X., Yu, B., Han, Y., Wang, X., Wang, Z., Zhang, M., & Wang, H. (2024) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14798 · Cited by 30 · see citing works
Cross-species systems analysis identifies gene networks differentially altered by sleep loss and depression
Scarpa, J. R., Jiang, P., Gao, V. D., Fitzpatrick, K., Millstein, J., Olker, C. J., Gotter, A. L., Winrow, C. J., Renger, J. J., Kasarskis, A., et al. (2018) · Science Advances · doi:10.1126/sciadv.aat1294 · Cited by 28 · see citing works
Effects of circadian misalignment on sleep in mice
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The sleep-wake distribution contributes to the peripheral rhythms in PERIOD-2
Hoekstra, M. M., Jan, M., Katsioudi, G., Emmenegger, Y., & Franken, P. (2021) · eLife · doi:10.7554/elife.69773 · Cited by 28 · see citing works
Recent advances in understanding the genetics of sleep
Jan, M., O’Hara, B. F., & Franken, P. (2020) · F1000Research · doi:10.12688/f1000research.22028.1 · Cited by 31 · see citing works
Sleep Modelling across Physiological Levels
Postnova, S. (2019) · Clocks & Sleep · doi:10.3390/clockssleep1010015 · Cited by 28 · see citing works
Understanding Quantitative Circadian Regulations Are Crucial Towards Advancing Chronotherapy
Chowdhury, D., Wang, C., Lü, A., & Zhu, H. (2019) · Cells · doi:10.3390/cells8080883 · Cited by 24 · see citing works
Circadian Clock, Glucocorticoids and NF-κB Signaling in Neuroinflammation- Implicating Glucocorticoid Induced Leucine Zipper as a Molecular Link
Srinivasan, M., & Walker, C. L. (2022) · ASN NEURO · doi:10.1177/17590914221120190 · Cited by 25 · see citing works
Tired and stressed: Examining the need for sleep
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Chronotype and a PERIOD3 variable number tandem repeat polymorphism in Han Chinese pilots.
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Distinct feedback actions of behavioural arousal to the master circadian clock in nocturnal and diurnal mammals
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Unique transcriptional signatures of sleep loss across independently evolved cavefish populations
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Parkinson’s Disease is Associated with Dysregulations of a Dopamine-Modulated Gene Network Relevant to Sleep and Affective Neurobehaviors in the Striatum
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Mitochondrial autophagy in the sleeping brain
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The after-hours circadian mutant has reduced phenotypic plasticity in behaviors at multiple timescales and in sleep homeostasis
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Cross talk mechanism of disturbed sleep patterns in neurological and psychological disorders
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Keep Your Mask On: The Benefits of Masking for Behavior and the Contributions of Aging and Disease on Dysfunctional Masking Pathways
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How does healthy aging impact on the circadian clock?
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Cell adhesion molecules and sleep
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Model integration of circadian- and sleep-wake-driven contributions to rhythmic gene expression reveals distinct regulatory principles
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The endogenous circadian clock programs animals to eat at certain times of the 24-hour day: What if we ignore the clock?
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Genetics and Genomic Basis of Sleep in Healthy Humans
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PER3 gene regulation of sleep-wake behavior as a function of latitude
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Astrocyte Circadian Timekeeping in Brain Health and Neurodegeneration
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Terpenoids derived from Semen Ziziphi Spinosae oil enhance sleep by modulating neurotransmitter signaling in mice
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Twist1 Is a TNF-Inducible Inhibitor of Clock Mediated Activation of Period Genes
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Sleep as spatiotemporal integration of biological processes that evolved to periodically reinforce neurodynamic and metabolic homeostasis: The 2m3d paradigm of sleep
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Sleep disturbance and dysregulation of circadian clock machinery in sudden sensorineural hearing loss
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Marine n-3 polyunsaturated fatty acids slow sleep impairment progression by regulating central circadian rhythms in type 2 diabetes
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Depriving Mice of Sleep also Deprives of Food
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Brain Clocks, Sleep, and Mood
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Cells have sex chromosomes and circadian clocks: Implications for organismal level functions
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Molecular targets and mechanisms involved in the action of Banxia Shumi decoction in insomnia treatment
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Noninvasive sleep monitoring in large-scale screening of knock-out mice reveals novel sleep-related genesPreprint
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The neurobiological mechanisms of photoperiod impact on brain functions: a comprehensive review
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Circadian Rhythm Mechanisms Underlying Convergent Adaptation of Unihemispheric Slow-Wave Sleep in Marine Mammals
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Mating duration of male Drosophila melanogaster – A novel genetic model to study interval timing function of human brain
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Deletion of the Circadian Clock Gene Per2 in the Whole Body, but Not in Neurons or Astroglia, Affects Sleep in Response to Sleep Deprivation
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Sleep deprivation and diet affect human GH gene expression in transgenic mice in vivo
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Genetic Association Studies in Restless Legs Syndrome: Risk Variants & Ethnic Differences
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Sleep Disturbances Linked to Genetic Disorders
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Gènes d’horloge : de la drosophile à l’homme
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Physiology of Normal Sleep
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Neurophysiology of Sleep and Wakefulness
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Clinical characterization of children and adolescents with ADHD and sleep disturbances
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Authors: Franken, P.
Affiliations: University of Lausanne (CH)
Corresponding author: Franken, Paul
ORCID: Franken, Paul
Venue: Current Opinion in Neurobiology
Publisher: Elsevier BV
Published: 2013-10
Volume: 23
Issue: 5
Pages: 864-872
ISSN: 0959-4388 (ISSN-L)
DOI: 10.1016/j.conb.2013.05.002
OpenAlex: W2079320127
Cited by: 125
References: 88
Citations by year: 2026: 4 · 2025: 4 · 2024: 11 · 2023: 5 · 2022: 14 · 2021: 8 · 2020: 13 · 2019: 16 · 2018: 9 · 2017: 10 · 2016: 15 · 2015: 9 · 2014: 6 · 2013: 1
FWCI: 1.23
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Current Opinion in Neurobiology (publishedVersion)
PubMed (publishedVersion)
IRIS (submittedVersion)
SERVAL (Université de Lausanne) (submittedVersion)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
Keywords: clock genes, sleep homeostasis, circadian clock, circadian rhythm, sleep-wake regulation, sleep deprivation, DNA binding, metabolic disorders, mice, Drosophila
MeSH terms: Animals, Homeostasis, Humans, Sleep, Wakefulness, CLOCK Proteins, Circadian Clocks

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A role for clock genes in sleep homeostasis

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