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Distinct Components of Photoperiodic Light Are Differentially Encoded by the Mammalian Circadian Clock.

ABSTRACT: Seasonal light cycles influence multiple physiological functions and are mediated through photoperiodic encoding by the circadian system. Despite our knowledge of the strong connection between seasonal light input and downstream circadian changes, less is known about the specific components of seasonal light cycles that are encoded and induce persistent changes in the circadian system. Using combinations of 3 T cycles (23, 24, 26 h) and 2 photoperiods per T cycle (long and short, with duty cycles scaled to each T cycle), we investigate the after-effects of entrainment to these 6 light cycles. We measure locomotor behavior duration (α), period (τ), and entrained phase angle (ψ) in vivo and SCN phase distribution (σ_φ), τ, and ψ ex vivo to refine our understanding of critical light components for influencing particular circadian properties. We find that both photoperiod and T-cycle length drive determination of in vivo ψ but differentially influence after-effects in α and τ, with photoperiod driving changes in α and photoperiod length and T-cycle length combining to influence τ. Using skeleton photoperiods, we demonstrate that in vivo ψ is determined by both parametric and nonparametric components, while changes in α are driven nonparametrically. Within the ex vivo SCN, we find that ψ and σ_φ of the PER2∷LUCIFERASE rhythm follow closely with their likely behavioral counterparts (ψ and α of the locomotor activity rhythm) while also confirming previous reports of τ after-effects of gene expression rhythms showing negative correlations with behavioral τ after-effects in response to T cycles. We demonstrate that within-SCN σ_φ changes, thought to underlie α changes in vivo, are induced primarily nonparametrically. Taken together, our results demonstrate that distinct components of seasonal light input differentially influence ψ, α, and τ and suggest the possibility of separate mechanisms driving the persistent changes in circadian behaviors mediated by seasonal light.

SUBMITTER: Tackenberg MC

PROVIDER: S-EPMC8281571 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundProstate cancer (PC) is one of the most common malignancies in males. Extensive and complex connections between circadian rhythm and cancer were found. Nonetheless, in PC, the potential role of the core components of the mammalian circadian clock (CCMCCs) in prognosis prediction has not been fully clarified.MethodsWe firstly collected 605 patients with PC from The Cancer Genome Atlas (TCGA) and the Gene Expression Omnibus (GEO) databases. Survival analysis was carried out for each CCMCC. Then, we investigated the prognostic ability of CCMCCs by Cox regression analysis. Independent prognostic signatures were extracted for the establishment of the circadian clock-based risk score model. We explored the predictive performance of the risk score model in the TCGA training cohort and the independent GEO dataset. Finally, the relationships between risk score and clinicopathological parameters, biological processes, and signaling pathways were evaluated.ResultsThe expression levels of CCMCCs were widely correlated with age, tumor status, lymph node status, disease-free survival (DFS), progression-free survival (PFS), and overall survival (OS). Nine circadian clock genes, including CSNK1D, BTRC, CLOCK, CSNK1E, FBXL3, PRKAA2, DBP, NR1D2, and RORB, were identified as vital prognostic factors in PC and were used to construct the circadian clock-based risk score model. For DFS, the area under the 3-year or 5-year receiver operating characteristic curves ranged from 0.728 to 0.821, suggesting better predictive performance. When compared with T3-4N1 stage, PC patients at T2N0 stage might be benefited more from the circadian clock-based risk score model. Furthermore, a high circadian clock-based risk score indicated shorter DFS (p < 0.0001), early progression (p < 0.0001), and higher 5-year death rate (p = 0.007) in PC. The risk score was related to tumor status (p < 0.001), lymph node status (p < 0.001), and ribosome-related biogenesis and pathways.ConclusionsThe vital roles of circadian clock genes in clinical outcomes were fully depicted. The circadian clock-based risk score model could reflect and predict the prognosis of patients with PC.

Project description:BACKGROUND: Most organisms have evolved a circadian clock in order to anticipate daily environmental changes and many of these organisms are also capable of sophisticated measurement of daylength (photoperiodism) that is used to regulate seasonal events such as diapause, migration and polymorphism. It has been generally accepted that the same elements are involved in both circadian (daily) and seasonal (annual) rhythms because both rely upon daily light-dark cycles. However, as reasonable as this sounds, there remains no conclusive evidence of such a molecular machinery in insects. We have approached this issue by using RNA interference (RNAi) in Riptortus pedestris. RESULTS: The cuticle deposition rhythm exhibited the major properties of circadian rhythms, indicating that the rhythm is regulated by a circadian clock. RNAi directed against the circadian clock genes of period and cycle, which are negative and positive regulators in the circadian clock, respectively, disrupted the cuticle deposition rhythm and distinct cuticle layers were produced by these RNAi. Simultaneously, period RNAi caused the insect to avert diapause under a diapause-inducing photoperiod whereas cycle RNAi induced diapause under a diapause-averting photoperiod. The expression patterns of juvenile hormone-regulated genes and the application of juvenile hormone analogue suggested that neither ovarian development itself nor a downstream cascade of juvenile hormone secretion, were disturbed by period and cycle RNAi. CONCLUSIONS: This study revealed that the circadian clock genes are crucial not only for daily rhythms but also for photoperiodic diapause. RNAi directed against period and cycle had opposite effects not only in the circadian cuticle deposition rhythm but also in the photoperiodic diapause. These RNAi also had opposite effects on juvenile hormone-regulated gene expression. It is still possible that the circadian clock genes pleiotropically affect ovarian development but, based on these results, we suggest that the circadian clock operated by the circadian clock genes, period and cycle, governs seasonal timing as well as the daily rhythms.

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Distinct Components of Photoperiodic Light Are Differentially Encoded by the Mammalian Circadian Clock.

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