Hippocampal spine changes across the sleep–wake cycle: corticosterone and kinases

Ikeda, Motoko; Hojo, Yasushi; Komatsuzaki, Yoshimasa; Okamoto, Masahiro; Kato, Asami; Takeda, Taishi; Kawato, Suguru

doi:10.1530/joe-15-0078

Cited by 42 publications

(46 citation statements)

References 65 publications

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“…For many synaptic components, diurnal and/or circadian rhythm of gene expression, modified gene expression in clock mutant models, DNA binding, and transcriptional activation by clock transcription factors suggest they are clock‐controlled genes. This implies a major role of the clock molecular machinery in shaping neuronal communication and synaptic plasticity, which is also supported by circadian studies of cellular correlates of synaptic plasticity (Chaudhury et al., ; Ikeda et al., ). Importantly, such a role may also support clock‐regulated transcriptional control in neurodevelopment, in aging, as well as in neuropsychiatric and neurological diseases, because of the established functions of synaptic components in these aspects (Akaneya et al., ; Avila et al., ; Südhof, ).…”

Section: Discussionmentioning

confidence: 74%

“…In the brain, circadian rhythms can be driven by changes in neuronal communication, which includes structural and functional modifications of the synapse, commonly termed synaptic plasticity. In fact, several measures of synaptic plasticity like LTP (long‐term potentiation) or changes in spine densities have been shown to follow a 24‐h rhythm (Chaudhury, Wang, & Colwell, ; Ikeda et al., ). Moreover, mouse models with repressed clock genes show altered LTP parameters, such as decreased potentiation at hippocampal Schaffer‐collateral synapses after high‐frequency stimulation when measured around the middle of the light period (Wardlaw et al., ).…”

Section: Introductionmentioning

confidence: 99%

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Transcriptional control of synaptic components by the clock machinery

Hannou

Roy

Roig

et al. 2019

Eur J of Neuroscience

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Circadian rhythms are generated in mammals by a central clock located in the suprachiasmatic nucleus of the hypothalamus, which regulates the homeostasis of many biological processes. At the molecular level, the regulation of circadian rhythms is under the control of transcriptional‐translational feedback loops composed of clock factors, including transcription factors. In the brain, synaptic plasticity has been shown to vary with a 24‐h rhythm. Also, when measured at a given time‐of‐day, synaptic plasticity has been observed to be disrupted by dysregulation of clock factors. This could suggest a regulation of synaptic functions by the clock machinery. Interestingly, many studies provide support for direct and indirect transcriptional regulation by core clock factors, including rhythmic gene expression, for a variety of synaptic components. Indeed, the gene of several neuropeptides, neurotransmitter regulators, receptors and transporters, ion channels, vesicle proteins, and adhesion and scaffolding molecules present evidence to be clock‐controlled. We here present, while considering different regions of the mammalian brain, an overview of the extent of the transcriptional control of synaptic components by the clock machinery.

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Section: Discussionmentioning

confidence: 74%

Section: Introductionmentioning

confidence: 99%

Transcriptional control of synaptic components by the clock machinery

Hannou

Roy

Roig

et al. 2019

Eur J of Neuroscience

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“…Along these lines, rats experience a rapid increase in dendritic spine density of CA1 pyramidal neurons shortly after entering the dark phase and their awake state, an effect that is mediated by various kinase pathways including MAPK/ERK, PKA, and PKC (39). Moreover, there is evidence that the sleep–wake cycle, which is coordinated by the circadian timing system, is linked to structural plasticity within the hippocampus and memory processes (40).…”

Section: Discussionmentioning

confidence: 99%

Phosphoproteome Profiling Reveals Circadian Clock Regulation of Posttranslational Modifications in the Murine Hippocampus

Chiang

Mehta

et al. 2017

Front. Neurol.

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The circadian clock is an endogenous oscillator that drives daily rhythms in physiology, behavior, and gene expression. The underlying mechanisms of circadian timekeeping are cell-autonomous and involve oscillatory expression of core clock genes that is driven by interconnecting transcription-translation feedback loops (TTFLs). Circadian clock TTFLs are further regulated by posttranslational modifications, in particular, phosphorylation. The hippocampus plays an important role in spatial memory and the conversion of short-to long-term memory. Several studies have reported the presence of a peripheral oscillator in the hippocampus and have highlighted the importance of circadian regulation in memory formation. Given the general importance of phosphorylation in circadian clock regulation, we performed global quantitative proteome and phosphoproteome analyses of the murine hippocampus across the circadian cycle, applying spiked-in labeled reference and high accuracy mass spectrometry (MS). Of the 3,052 proteins and 2,868 phosphosites on 1,368 proteins that were accurately quantified, 1.7% of proteins and 5.2% of phosphorylation events exhibited time-of-day-dependent expression profiles. The majority of circadian phosphopeptides displayed abrupt fluctuations at mid-to-late day without underlying rhythms of protein abundance. Bioinformatic analysis of cyclic phosphorylation events revealed their diverse distribution in different biological pathways, most notably, cytoskeletal organization and neuronal morphogenesis. This study provides the first large-scale, quantitative MS analysis of the circadian phosphoproteome and proteome of the murine hippocampus and highlights the significance of rhythmic regulation at the posttranslational level in this peripheral oscillator. In addition to providing molecular insights into the hippocampal circadian clock, our results will assist in the understanding of genetic factors that underlie rhythms-associated pathological states of the hippocampus.

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“…Indeed, dexamethasonetreated mice showed neurological and memory deficits that could be ameliorated with corticosterone substitution (Liston & Gan 2011, Liston et al 2013. The finding that corticosterone acts via changes to hippocampal neuronal spines during the sleep-wake cycle received the Society for Endocrinology's 2015 award for the best article published in Journal of Endocrinology (Ikeda et al 2015).…”

Section: Cellular and Behavioural Studiesmentioning

confidence: 99%

30 YEARS OF THE MINERALOCORTICOID RECEPTOR: The brain mineralocorticoid receptor: a saga in three episodes

Joëls

Kloet

2017

Journal of Endocrinology

118

109

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In 1968, Bruce McEwen discovered that 3 H-corticosterone administered to adrenalectomised rats is retained in neurons of hippocampus rather than those of hypothalamus. This discovery signalled the expansion of endocrinology into the science of higher brain regions. With this in mind, our contribution highlights the saga of the brain mineralocorticoid receptor (MR) in three episodes. First, the precloning era dominated by the conundrum of two types of corticosterone-binding receptors in the brain, which led to the identification of the high-affinity corticosterone receptor as the 'promiscuous' MR cloned in 1987 by Jeff Arriza and Ron Evans in addition to the classical glucocorticoid receptor (GR). Then, the post-cloning period aimed to disentangle the function of the brain MR from that of the closely related GR on different levels of biological complexity. Finally, the synthesis section that highlights the two faces of brain MR: Salt and Stress. 'Salt' refers to the regulation of salt appetite, and reciprocal arousal, motivation and reward, by a network of aldosterone-selective MR-expressing neurons projecting from nucleus tractus solitarii (NTS) and circumventricular organs. 'Stress' is about the limbic-forebrain nuclear and membrane MRs, which act as a switch in the selection of the best response to cope with a stressor. For this purpose, activation of the limbic MR promotes selective attention, memory retrieval and the appraisal process, while driving emotional expressions of fear and aggression. Subsequently, rising glucocorticoid concentrations activate GRs in limbic-forebrain circuitry underlying executive functions and memory storage, which contribute in balance with MR-mediated actions to homeostasis, excitability and behavioural adaptation.

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Hippocampal spine changes across the sleep–wake cycle: corticosterone and kinases

Cited by 42 publications

References 65 publications

Transcriptional control of synaptic components by the clock machinery

Transcriptional control of synaptic components by the clock machinery

Phosphoproteome Profiling Reveals Circadian Clock Regulation of Posttranslational Modifications in the Murine Hippocampus

30 YEARS OF THE MINERALOCORTICOID RECEPTOR: The brain mineralocorticoid receptor: a saga in three episodes

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