Transcriptome Analysis Reveals Altered Expression of Memory and Neurotransmission Associated Genes in the REM Sleep Deprived Rat Brain

Narwade, Santosh C.; Mallick, Birendra Nath; Deobagkar, Deepti D.

doi:10.3389/fnmol.2017.00067

Cited by 24 publications

(16 citation statements)

References 73 publications

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“…This result, as well as previous findings in humans (53, 54), suggest that these phenomena share common causal mechanisms. Hypothalamic neuropeptides, such as vasoactive intestinal peptide (VIP), arginine vasopressin (AVP), and melanin-concentrating hormone (MCH), whose encoding genes were down-regulated in the present study, are potential candidates for orchestrating this association because they have been implicated in the regulation of REMS (55–58) and the HPA axis (59, 60). In humans, increased REMS (61) and HPA axis dysregulation (13) have been shown to correlate with remission and recovery in major depressive disorder.…”

Section: Discussionmentioning

confidence: 79%

REM sleep’s unique associations with corticosterone regulation, apoptotic pathways, and behavior in chronic stress in mice

Nollet

Hicks

McCarthy

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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One of sleep’s putative functions is mediation of adaptation to waking experiences. Chronic stress is a common waking experience; however, which specific aspect of sleep is most responsive, and how sleep changes relate to behavioral disturbances and molecular correlates remain unknown. We quantified sleep, physical, endocrine, and behavioral variables, as well as the brain and blood transcriptome in mice exposed to 9 weeks of unpredictable chronic mild stress (UCMS). Comparing 46 phenotypic variables revealed that rapid–eye-movement sleep (REMS), corticosterone regulation, and coat state were most responsive to UCMS. REMS theta oscillations were enhanced, whereas delta oscillations in non-REMS were unaffected. Transcripts affected by UCMS in the prefrontal cortex, hippocampus, hypothalamus, and blood were associated with inflammatory and immune responses. A machine-learning approach controlling for unspecific UCMS effects identified transcriptomic predictor sets for REMS parameters that were enriched in 193 pathways, including some involved in stem cells, immune response, and apoptosis and survival. Only three pathways were enriched in predictor sets for non-REMS. Transcriptomic predictor sets for variation in REMS continuity and theta activity shared many pathways with corticosterone regulation, in particular pathways implicated in apoptosis and survival, including mitochondrial apoptotic machinery. Predictor sets for REMS and anhedonia shared pathways involved in oxidative stress, cell proliferation, and apoptosis. These data identify REMS as a core and early element of the response to chronic stress, and identify apoptosis and survival pathways as a putative mechanism by which REMS may mediate the response to stressful waking experiences.

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Section: Discussionmentioning

confidence: 79%

REM sleep’s unique associations with corticosterone regulation, apoptotic pathways, and behavior in chronic stress in mice

Nollet

Hicks

McCarthy

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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“…Some studies have been conducted in rats and mice. In a recent REMSD study, changes in chromatin assembly, methylation of genes involved in learning and memory, regulation of synaptic transmission, neuronal plasticity and neurohypophyseal hormone synthesis in rat brain have been reported, 124 which help explain REMSD-associated long-term behavioral and other changes described in this review.…”

Section: Contribution Of Remsd Studies To Understand Rems Regulation mentioning

confidence: 81%

Relevance of deprivation studies in understanding rapid eye movement sleep

Mehta

Khan

Mallick

2018

NSS

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Rapid eye movement sleep (REMS) is a unique phenomenon essential for maintaining normal physiological processes and is expressed at least in species higher in the evolution. The basic scaffold of the neuronal network responsible for REMS regulation is present in the brainstem, which may be directly or indirectly influenced by most other physiological processes. It is regulated by the neurons in the brainstem. Various manipulations including chemical, elec-trophysiological, lesion, stimulation, behavioral, ontogenic and deprivation studies have been designed to understand REMS genesis, maintenance, physiology and functional significance. Although each of these methods has its significance and limitations, deprivation studies have contributed significantly to the overall understanding of REMS. In this review, we discuss the advantages and limitations of various methods used for REMS deprivation (REMSD) to understand neural regulation and physiological significance of REMS. Among the deprivation strategies, the flowerpot method is by far the method of choice because it is simple and convenient, exploits physiological parameter (muscle atonia) for REMSD and allows conducting adequate controls to overcome experimental limitations as well as to rule out nonspecific effects. Notwithstanding, a major criticism that the flowerpot method faces is that of perceived stress experienced by the experimental animals. Nevertheless, we conclude that like most methods, particularly for in vivo behavioral studies, in spite of a few limitations, given the advantages described above, the flowerpot method is the best method of choice for REMSD studies.

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“…Further, twins with distinct diurnal preferences have different DNA methylation patterns (Wong et al, 2015 ) and short sleepers (<6.8 h) have altered DNA methylation patterns in 52 genes when compared to long sleepers (>7.8 h; Huang et al, 2017 ). In rats, deprivation of rapid eye movement (REM) sleep results in a significant change in the expression of genes related to DNA methylation (Narwade et al, 2017 ). There is also substantial evidence linking the methylation status of circadian clock genes and sleep loss (Qureshi and Mehler, 2014 ).…”

Section: Sleep and The Methylomementioning

confidence: 99%

Sleep Deprivation and the Epigenome

Gaine

Chatterjee

Abel

2018

Front. Neural Circuits

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Sleep deprivation disrupts the lives of millions of people every day and has a profound impact on the molecular biology of the brain. These effects begin as changes within a neuron, at the DNA and RNA level, and result in alterations in neuronal plasticity and dysregulation of many cognitive functions including learning and memory. The epigenome plays a critical role in regulating gene expression in the context of memory storage. In this review article, we begin by describing the effects of epigenetic alterations on the regulation of gene expression, focusing on the most common epigenetic mechanisms: (i) DNA methylation; (ii) histone modifications; and (iii) non-coding RNAs. We then discuss evidence suggesting that sleep loss impacts the epigenome and that these epigenetic alterations might mediate the changes in cognition seen following disruption of sleep. The link between sleep and the epigenome is only beginning to be elucidated, but clear evidence exists that epigenetic alterations occur following sleep deprivation. In the future, these changes to the epigenome could be utilized as biomarkers of sleep loss or as therapeutic targets for sleep-related disorders.

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Transcriptome Analysis Reveals Altered Expression of Memory and Neurotransmission Associated Genes in the REM Sleep Deprived Rat Brain

Cited by 24 publications

References 73 publications

REM sleep’s unique associations with corticosterone regulation, apoptotic pathways, and behavior in chronic stress in mice

REM sleep’s unique associations with corticosterone regulation, apoptotic pathways, and behavior in chronic stress in mice

Relevance of deprivation studies in understanding rapid eye movement sleep

Sleep Deprivation and the Epigenome

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