Cellular Circadian Clocks in Mood Disorders

McCarthy, Michael J.; Welsh, David K.

doi:10.1177/0748730412456367

Cited by 203Circadian rhythm and melatoninBipolar Disorder and TreatmentTreatment of Major Depression

Cellular Circadian Clocks in Mood Disorders

McCarthy, Michael J., Welsh, David K.·2012·Journal of Biological Rhythms

DOI 10.1177/0748730412456367

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Abstract

Bipolar disorder (BD) and major depressive disorder (MDD) are heritable neuropsychiatric disorders associated with disrupted circadian rhythms. The hypothesis that circadian clock dysfunction plays a causal role in these disorders has endured for decades but has been difficult to test and remains controversial. In the meantime, the discovery of clock genes and cellular clocks has revolutionized our understanding of circadian timing. Cellular circadian clocks are located in the suprachiasmatic nucleus (SCN), the brain’s primary circadian pacemaker, but also throughout the brain and peripheral tissues. In BD and MDD patients, defects have been found in SCN-dependent rhythms of body temperature and melatonin release. However, these are imperfect and indirect indicators of SCN function. Moreover, the SCN may not be particularly relevant to mood regulation, whereas the lateral habenula, ventral tegmentum, and hippocampus, which also contain cellular clocks, have established roles in this regard. Dysfunction in these non-SCN clocks could contribute directly to the pathophysiology of BD/MDD. We hypothesize that circadian clock dysfunction in non-SCN clocks is a trait marker of mood disorders, encoded by pathological genetic variants. Because network features of the SCN render it uniquely resistant to perturbation, previous studies of SCN outputs in mood disorders patients may have failed to detect genetic defects affecting non-SCN clocks, which include not only mood-regulating neurons in the brain but also peripheral cells accessible in human subjects. Therefore, reporters of rhythmic clock gene expression in cells from patients or mouse models could provide a direct assay of the molecular gears of the clock, in cellular clocks that are likely to be more representative than the SCN of mood-regulating neurons in patients. This approach, informed by the new insights and tools of modern chronobiology, will allow a more definitive test of the role of cellular circadian clocks in mood disorders.

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A major component of many mood, anxiety and psychotic disorders is a disrupted sleep-wake cycle.
“A major component of many mood, anxiety and psychotic disorders is a disrupted sleep–wake cycle183–188”
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Habenula Volume in Bipolar Disorder and Major Depressive Disorder: A High-Resolution Magnetic Resonance Imaging Study
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The MATRICS Consensus Cognitive Battery in Patients with Bipolar I Disorder
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Replicable differences in preferred circadian phase between bipolar disorder patients and control individuals
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A Survey of Genomic Studies Supports Association of Circadian Clock Genes with Bipolar Disorder Spectrum Illnesses and Lithium Response
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Alterations in arginine vasopressin neurons in the suprachiasmatic nucleus in depression
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Remitted major depression is characterized by reward network hyperactivation during reward anticipation and hypoactivation during reward outcomes
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Lithium Impacts on the Amplitude and Period of the Molecular Circadian Clockwork
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Kinases and phosphatases in the mammalian circadian clock
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Treatment of a Rapidly Cycling Bipolar Patient by Using Extended Bed Rest and Darkness to Stabilize the Timing and Duration of Sleep
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Circadian firing-rate rhythms and light responses of rat habenular nucleus neurons in vivo and in vitro
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A Circadian Clock in the Olfactory Bulb Controls Olfactory Responsivity
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Inter-Individual Differences In Habitual Sleep Timing and Entrained Phase of Endogenous Circadian Rhythms of BMAL1, PER2 and PER3 mRNA in Human Leukocytes
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CRY2 Is Associated with Depression
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Genome-Wide Association Scan of Trait Depression
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A length polymorphism in the circadian clock gene Per3 influences age at onset of bipolar disorder
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Perinatal photoperiod imprints the circadian clock
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Lithium slows rat circadian activity rhythms
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Effects of Stress
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PER2 variantion is associated with depression vulnerability
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Fluoxetine Modulates the Circadian Biological Clock via Phase Advances of Suprachiasmatic Nucleus Neuronal Firing
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Potentiation of antidepressant medications by phase advance of the sleep-wake cycle
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Increased Medial Orbitofrontal and Amygdala Activation: Evidence for a Systems-Level Endophenotype of Bipolar I Disorder
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Evidence for genetic association of RORB with bipolar disorder
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Soluble 3′,6-Substituted Indirubins with Enhanced Selectivity toward Glycogen Synthase Kinase -3 Alter Circadian Period
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Assessment of circadian function in fibroblasts of patients with bipolar disorder
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Circadian oscillators in the epithalamus
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Circadian temperature and cortisol rhythms during a constant routine are phase-delayed in hypersomnic winter depression
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The Physiological Period Length of the Human Circadian Clock In Vivo Is Directly Proportional to Period in Human Fibroblasts
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Subjective Well-Being Is Modulated by Circadian Phase, Sleep Pressure, Age, and Gender
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The circadian Clock mutation increases exploratory activity and escape-seeking behavior
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Relation between morningness–eveningness score and depressive symptoms among patients with delayed sleep phase syndrome
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Affective responses to changes in day length in Siberian hamsters (Phodopus sungorus)
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The psychological aspects of patients with delayed sleep phase syndrome (DSPS)
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Valproic Acid Phase Shifts the Rhythmic Expression of PERIOD2::LUCIFERASE
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Functional genetic variation in the Rev-Erbαpathway and lithium response in the treatment of bipolar disorder
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Self-citation
CLOCK is suggested to associate with comorbid alcohol use and depressive disorders
Sjoholm, L. K., Kovanen, L., Saarikoski, S. T., Schalling, M., & Lavebratt, C. (2010) · Journal of Circadian Rhythms · doi:10.1186/1740-3391-8-1 · Cited by 97 · see citing works
Real-Time Reporting of Circadian-Regulated Gene Expression by Luciferase Imaging in Plants and Mammalian Cells
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Sleep and Sleep-Wake Manipulations in Bipolar Depression
Riemann, D. W., Voderholzer, U., & Berger, T. (2002) · Neuropsychobiology · doi:10.1159/000049255 · Cited by 91 · see citing works
Novel neurons in ventral tegmental area fire selectively during the active phase of the diurnal cycle
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Persistent Cell-Autonomous Circadian Oscillations in Fibroblasts Revealed by Six-Week Single-Cell Imaging of PER2::LUC Bioluminescence
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Period 2 regulates neural stem/progenitor cell proliferation in the adult hippocampus
Borgs, L., Beukelaers, P., Vandenbosch, R., Nguyen, L., Moonen, G., Maquet, P., Albrecht, U., Belachew, S. M., & Malgrange, B. (2009) · BMC Neuroscience · doi:10.1186/1471-2202-10-30 · Cited by 84 · see citing works
Serotonergic activation potentiates light resetting of the main circadian clock and alters clock gene expression in a diurnal rodent
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CRY2 Is Associated with Rapid Cycling in Bipolar Disorder Patients
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The methamphetamine-sensitive circadian oscillator does not employ canonical clock genes
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Association between CLOCK 3111T/C and preferred circadian phase in Korean patients with bipolar disorder
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Delayed sleep phase syndrome is related to seasonal affective disorder
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Coming to grips with complex disorders: Genetic risk prediction in bipolar disorder using panels of genes identified through convergent functional genomics
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A Forced Desynchrony Study of Circadian Pacemaker Characteristics in Seasonal Affective Disorder
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Lithium lengthens circadian period in a diurnal primate, Saimiri sciureus
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Effects of bright light treatment on depression- and anxiety-like behaviors of diurnal rodents maintained on a short daylight schedule
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Assessment of circadian rhythms in humans: comparison of real-time fibroblast reporter imaging with plasma melatonin
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Nuclear Receptor Rev-Erb- α Circadian Gene Variants and Lithium Carbonate Prophylaxis in Bipolar Affective Disorder
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Time-of-Day-Dependent Enhancement of Adult Neurogenesis in the Hippocampus
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Rhythmic expression of per1 in the dentate gyrus is suppressed by corticosterone: Implications for neurogenesis
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CLOCK may Predict the Response to Fluvoxamine Treatment in Japanese Major Depressive Disorder Patients
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Rhythms of life: circadian disruption and brain disorders across the lifespan
Logan, R. W., & McClung, C. A. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0088-y · Cited by 713 · see citing works
Circadian misalignment and health
Baron, K. G., & Reid, K. J. (2014) · International Review of Psychiatry · doi:10.3109/09540261.2014.911149 · Cited by 645 · see citing works
Health Consequences of Circadian Disruption in Humans and Animal Models
Evans, J. A., & Davidson, A. J. (2013) · Progress in Molecular Biology and Translational Science · doi:10.1016/b978-0-12-396971-2.00010-5 · Cited by 291 · see citing works
Genetic Disruption of Circadian Rhythms in the Suprachiasmatic Nucleus Causes Helplessness, Behavioral Despair, and Anxiety-like Behavior in Mice
Landgraf, D., Long, J. E., Proulx, C. D., Barandas, R., Malinow, R., & Welsh, D. K. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.03.1050 · Cited by 212 · see citing works
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Dopamine: A Modulator of Circadian Rhythms in the Central Nervous System
Korshunov, K. S., Blakemore, L. J., & Trombley, P. Q. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00091 · Cited by 173 · see citing works
Genetic and clinical factors predict lithium’s effects on PER2 gene expression rhythms in cells from bipolar disorder patients
McCarthy, M. J., Wei, H., Marnoy, Z., Darvish, R. M., McPhie, D. L., Cohen, B. M., & Welsh, D. K. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.90 · Cited by 137 · see citing works
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Animal models of bipolar mania: The past, present and future
Logan, R. W., & McClung, C. A. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2015.08.041 · Cited by 136 · see citing works
Neurobiological and behavioral mechanisms of circadian rhythm disruption in bipolar disorder: A critical multi‐disciplinary literature review and agenda for future research from the ISBD task force on chronobiology
McCarthy, M. J., Gottlieb, J. F., Gonzalez, R., McClung, C. A., Alloy, L. B., Cain, S., Dulcis, D., Etain, B., Frey, B. N., Garbazza, C., et al. (2022) · Bipolar Disorders · doi:10.1111/bdi.13165 · Cited by 136 · see citing works
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Learning from the past and looking to the future: emerging perspectives for improving the treatment of psychiatric disorders
Millan, M. J., Goodwin, G. M., Meyer-Lindenberg, A., & Ove Ögren, S. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.01.016 · Cited by 132 · see citing works
Molecular aspects of circadian pharmacology and relevance for cancer chronotherapy
Ozturk, N., Ozturk, D., Kavakli, I. H., & Okyar, A. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18102168 · Cited by 106 · see citing works
Precision medicine for mood disorders: objective assessment, risk prediction, pharmacogenomics, and repurposed drugs
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Dim light at night increases depressive-like responses in male C3H/HeNHsd mice
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Authors: McCarthy, M. J., & Welsh, D. K.
Affiliations: University of California San Diego (US)
Corresponding author: Welsh, David K.
ORCID: McCarthy, Michael J.
Welsh, David K.
Venue: Journal of Biological Rhythms
Publisher: SAGE Publications
Published: 2012-09-25
Volume: 27
Issue: 5
Pages: 339-352
ISSN: 0748-7304 (ISSN-L)
1552-4531
DOI: 10.1177/0748730412456367
OpenAlex: W2011214288
Cited by: 203
References: 156
Citations by year: 2026: 9 · 2025: 9 · 2024: 11 · 2023: 9 · 2022: 7 · 2021: 12 · 2020: 11 · 2019: 16 · 2018: 14 · 2017: 24 · 2016: 22 · 2015: 24 · 2014: 17 · 2013: 18
FWCI: 8.42
Type: journal article
Language: en
Open access: closed
Licence: journals.sagepub.com/page/policies/text-and-data-mining-license (tdm)
Locations: Journal of Biological Rhythms (publishedVersion)
PubMed (publishedVersion)
Funders: U.S. Department of Veterans Affairs (IK2 BX001275)
National Alliance for Research on Schizophrenia and Depression
National Institute of Mental Health (R01MH082945)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Health Sciences › Medicine › Psychiatry and Mental health › Bipolar Disorder and Treatment
Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
Keywords: mood disorders, bipolar disorder, major depressive disorder, circadian rhythm disruption, clock genes, suprachiasmatic nucleus, lateral habenula, ventral tegmental area, hippocampus, melatonin, body temperature rhythm, genetic variants, chronobiology
MeSH terms: Amygdala, Animals, Antidepressive Agents, Bipolar Disorder, Depressive Disorder, Major, Major Depressive Disorder, Gyrus Cinguli, Hippocampus, Humans, Light, Periaqueductal Gray, Suprachiasmatic Nucleus, Lithium Compounds, Habenula, Models, Animal, Mice, Genome-Wide Association Study, CLOCK Proteins, Circadian Clocks

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Cellular Circadian Clocks in Mood Disorders

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