Entrainment of the Circadian Clock in Neural Stem Cells by Epidermal Growth Factor is Closely Associated with ERK1/2-mediated Induction of Multiple Clock-related Genes

Mogi, Asuka; Yomoda, Ryo; Kimura, Syunya; Tsushima, Chisato; Takouda, Jun; Sawauchi, Miho; Maekawa, Tomoko; Ohta, Hidenobu; Nishino, Satoshi; Kurita, Masatake; Mano, Nariyasu; Osumi, Noriko; Moriya, Takuya

doi:10.1016/j.neuroscience.2018.02.045

Cited by 8 publications

(6 citation statements)

References 69 publications

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“…A genome-wide study had found a strong relationship between sleep deprivation and the expression of PER genes in MDD and bipolar disorder patients (111). Moreover, the role of the circadian clock in the homeostasis of stem cells and in the regulation of cellular development including differentiation across tissue subtypes is supported by numerous studies (112)(113)(114). And the circadian rhythm disorder may disrupt normal sleep rhythm, which promotes myelination and oligodendrocyte precursor cells proliferation and is associated with higher expression of genes coding for phospholipid synthesis and myelination in oligodendrocytes (115)(116)(117).…”

Section: Discussionmentioning

confidence: 99%

Per1 gene polymorphisms influence the relationship between brain white matter microstructure and depression risk

et al. 2022

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BackgroundCircadian rhythm was involved in the pathogenesis of depression. The detection of circadian genes and white matter (WM) integrity achieved increasing focus for early prediction and diagnosis of major depressive disorder (MDD). This study aimed to explore the effects of PER1 gene polymorphisms (rs7221412), one of the key circadian genes, on the association between depressive level and WM microstructural integrity.Materials and methodsDiffusion tensor imaging scanning and depression assessment (Beck Depression Inventory, BDI) were performed in 77 healthy college students. Participants also underwent PER1 polymorphism detection and were divided into the AG group and AA group. The effects of PER1 genotypes on the association between the WM characteristics and BDI were analyzed using tract-based spatial statistics method.ResultsCompared with homozygous form of PER1 gene (AA), more individuals with risk allele G of PER1 gene (AG) were in depression state with BDI cutoff of 14 (χ2 = 7.37, uncorrected p = 0.007). At the level of brain imaging, the WM integrity in corpus callosum, internal capsule, corona radiata and fornix was poorer in AG group compared with AA group. Furthermore, significant interaction effects of genotype × BDI on WM characteristics were observed in several emotion-related WM tracts. To be specific, the significant relationships between BDI and WM characteristics in corpus callosum, internal capsule, corona radiata, fornix, external capsule and sagittal stratum were only found in AG group, but not in AA group.ConclusionOur findings suggested that the PER1 genotypes and emotion-related WM microstructure may provide more effective measures of depression risk at an early phase.

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Section: Discussionmentioning

confidence: 99%

Per1 gene polymorphisms influence the relationship between brain white matter microstructure and depression risk

et al. 2022

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“…IGF-1 entrains the circadian clock in the liver, highlighting the two-way relationship between circadian-regulated targets and the circadian clock itself ( 94 – 96 ). Similarly, nerve growth factor (NGF) was found to entrain the circadian clock in hamsters, and epidermal growth factor (EGF) is seen to induce clock gene expression in neural stem cells ( 97 – 99 ). Likewise, fibroblast growth factor (FGF) and platelet-derived growth factor (PDGF) induce robust PER1 expression in murine fibroblasts ( 100 ).…”

Section: Circadian Modification Of the Tumor Microenvironmentmentioning

confidence: 99%

Review: therapeutic approaches for circadian modulation of the glioma microenvironment

Nettnin,

Nguyen,

Arana

et al. 2023

Front. Oncol.

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High-grade gliomas are malignant brain tumors that are characteristically hard to treat because of their nature; they grow quickly and invasively through the brain tissue and develop chemoradiation resistance in adults. There is also a distinct lack of targeted treatment options in the pediatric population for this tumor type to date. Several approaches to overcome therapeutic resistance have been explored, including targeted therapy to growth pathways (ie. EGFR and VEGF inhibitors), epigenetic modulators, and immunotherapies such as Chimeric Antigen Receptor T-cell and vaccine therapies. One new promising approach relies on the timing of chemotherapy administration based on intrinsic circadian rhythms. Recent work in glioblastoma has demonstrated temporal variations in chemosensitivity and, thus, improved survival based on treatment time of day. This may be due to intrinsic rhythms of the glioma cells, permeability of the blood brain barrier to chemotherapy agents, the tumor immune microenvironment, or another unknown mechanism. We review the literature to discuss chronotherapeutic approaches to high-grade glioma treatment, circadian regulation of the immune system and tumor microenvironment in gliomas. We further discuss how these two areas may be combined to temporally regulate and/or improve the effectiveness of immunotherapies.

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“…Lack of Bmal-1 promoter activation by EGF is surprising in light of its effects on clock gene expression via the Per-2 promoter in other cell lines (9,21,22,25). Note that PER-2 hinders the Bmal-1 suppressor REV-ERB␣ from its inhibitory actions on this promoter.…”

Section: Igf-1 But Not Egf or Ngf Regulates Clock Gene Expression In mentioning

confidence: 99%

“…Clock gene expression regulating hormones are, thus, able to act as a zeitgeber for the cellular clock as shown for serum (12). EGF, did not entrain the clock in fibroblasts but in neuronal stem cells (9,21). NGF has been shown to entrain the clock in the suprachiasmatic nucleus of Syrian hamster (22,25).…”

mentioning

confidence: 90%

Insulin-like growth factor-1 acts as a zeitgeber on hypothalamic circadian clock gene expression via glycogen synthase kinase-3β signaling

Breit

Miek

Schredelseker

et al. 2018

Journal of Biological Chemistry

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Brain and muscle ARNT-like protein-1 (BMAL-1) is an important component of the cellular circadian clock. Proteins such as epidermal (EGF) or nerve growth factor (NGF) affect the cellular clock via extracellular signal-regulated kinases-1/2 (ERK-1/2) in NIH3T3 or neuronal stem cells, but no such data are available for the insulin-like growth factor-1 (IGF-1). The hypothalamus expresses receptors for all three growth factors, acts as a central circadian pacemaker, and releases hormones in a circadian fashion. However, little is known about growth factor-induced modulation of clock gene activity in hypothalamic cells. Here, we investigated effects of IGF-1, EGF, or NGF on the promoter in two hypothalamic cell lines. We found that only IGF-1 but not EGF or NGF enhanced activity of the promoter. Inhibition of ERK-1/2 activity did not affect IGF-1-induced promoter activation and all three growth factors similarly phosphorylated ERK-1/2, questioning a role for ERK-1/2 in controlling promoter activity. Of note, only IGF-1 induced sustained phosphorylation of glycogen synthase kinase-3β (GSK-3β). Moreover, the GSK-3β inhibitor lithium or siRNA-mediated GSK-3β knockdown diminished the effects of IGF-1 on the promoter. When IGF-1 was used in the context of temperature cycles entraining hypothalamic clock gene expression to a 24-h rhythm, it shifted the phase of promoter activity, indicating that IGF-1 functions as a zeitgeber for cellular hypothalamic circadian clocks. Our results reveal that IGF-1 regulates clock gene expression and that GSK-3β but not ERK-1/2 is required for the IGF-1-mediated regulation of the promoter in hypothalamic cells.

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Entrainment of the Circadian Clock in Neural Stem Cells by Epidermal Growth Factor is Closely Associated with ERK1/2-mediated Induction of Multiple Clock-related Genes

Cited by 8 publications

References 69 publications

Per1 gene polymorphisms influence the relationship between brain white matter microstructure and depression risk

Per1 gene polymorphisms influence the relationship between brain white matter microstructure and depression risk

Review: therapeutic approaches for circadian modulation of the glioma microenvironment

Insulin-like growth factor-1 acts as a zeitgeber on hypothalamic circadian clock gene expression via glycogen synthase kinase-3β signaling

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