Comparative transcriptomics of the Djungarian hamster hypothalamus during short photoperiod acclimation and spontaneous torpor

Haugg, Elena; Borner, Janus; Diedrich, Victoria; Herwig, Annika

doi:10.1002/2211-5463.13350

Cited by 10 publications

(16 citation statements)

References 101 publications

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“…A volcano plot of the whole SCN data shows large magnitude changes in expression in known hypothalamic photoperiod response genes downstream of the SCN, such as Lrat in the retinoic acid signaling pathway (Shearer et al, 2010) and Tshβ (Korf and Møller, 2021), Npvf (Dardente and Simonneaux, 2022), Dct (Dardente and Lomet, 2018), Dio2 (Korf and Møller, 2021), Tafa3 (Korf and Møller, 2021), and Slc16a2 (Ross et al, 2011) in the photoperiodic endocrine system (Fig 3), indicating that the photoperiod exposure indeed evoked a downstream photoperiodic response. Further, the direction of change agrees with multiple studies in mammals, with Lrat , Npvf , Tshβ , Dct , and Dio2 all reported to be upregulated in Long photoperiod (Dardente and Lomet, 2018; Haugg et al, 2022; Korf and Møller, 2021; Shearer et al, 2010).…”

Section: Resultssupporting

confidence: 89%

“…A volcano plot of the whole SCN data shows large magnitude changes in expression in known hypothalamic photoperiod response genes downstream of the SCN, such as Lrat in the retinoic acid signaling pathway [49] and Tshβ [50], Npvf [51], Dct [52], Dio2 [50], Tafa3 [50], and Slc16a2 [53] in the photoperiodic endocrine system (Fig 3), indicating that the photoperiod exposure indeed evoked a downstream photoperiodic response. Further, the direction of change agrees with multiple studies in mammals, with Lrat , Npvf , Tshβ , Dct , and Dio2 all reported to be upregulated in Long photoperiod [49,50,52,54]. To focus on genes robustly expressed in the SCN in our dataset, we used gene expression data from recent scRNA studies of SCN neurons for exploratory analysis [55,56].…”

Section: Resultssupporting

confidence: 63%

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Gene expression plasticity of the mammalian brain circadian clock in response to photoperiod

Cox,

Gianonni-Guzmán,

Cartailler

et al. 2024

Preprint

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Seasonal daylength, or circadian photoperiod, is a pervasive environmental signal that profoundly influences physiology and behavior. In mammals, the central circadian clock resides in the suprachiasmatic nuclei (SCN) of the hypothalamus and synchronizes, or entrains, physiology and behavior to the prevailing light cycle from retinal input. The process of entrainment induces considerable plasticity in the SCN, but the molecular mechanisms underlying SCN plasticity are incompletely understood. Entrainment to different photoperiods persistently alters the phase, waveform, period, and resetting properties of the SCN and its driven rhythms. To elucidate novel molecular mechanisms of photoperiod plasticity, we performed RNAseq on whole SCN dissected from mice raised in Long (LD 16:8) and Short (LD 8:16) photoperiods. Using differential rhythms analysis, we showed that fewer rhythmic genes were detected in Long photoperiod and that there was an overall phase advance of gene expression rhythms of 4-6 hours. However, a few genes showed significant phase delays, including GTP binding protein overexpressed in skeletal muscle (Gem), an SCN light responsive gene and light response modulator. Using differential expression analysis, we found significant expression changes in the clock-associated gene timeless circadian clock 1 (Timeless) and abundant changes in expression levels of SCN neural signaling genes related to light responses, neuropeptides, GABA, ion channels, and serotonin. Particularly striking were differences across photoperiods in the expression of the SCN neuropeptide signaling genes, prokineticin receptor 2 (Prokr2) and cholecystokinin (Cck), as well as convergent regulation of the expression of three SCN light response genes, dual specificity phosphatase 4 (Dusp4) and RAS, dexamethasone-induced 1 (Rasd1), andGem. Transcriptional modulation ofDusp4andRasd1,and phase regulation ofGem,are compelling candidate molecular mechanisms for photoperiod-induced plasticity in the SCN light response. Similarly, transcriptional modulation ofProkr2andCckmay critically support SCN neural network reconfiguration during photoperiodic entrainment. Our findings identify the SCN light response and neuropeptide signaling gene sets as rich substrates for elucidating novel mechanisms of photoperiod plasticity.

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Section: Resultssupporting

confidence: 89%

“…A volcano plot of the whole SCN data shows large magnitude changes in expression in known hypothalamic photoperiod response genes downstream of the SCN, such as Lrat in the retinoic acid signaling pathway [49] and Tshβ [50], Npvf [51], Dct [52], Dio2 [50], Tafa3 [50], and Slc16a2 [53] in the photoperiodic endocrine system (Fig 3), indicating that the photoperiod exposure indeed evoked a downstream photoperiodic response. Further, the direction of change agrees with multiple studies in mammals, with Lrat , Npvf , Tshβ , Dct , and Dio2 all reported to be upregulated in Long photoperiod [49,50,52,54]. To focus on genes robustly expressed in the SCN in our dataset, we used gene expression data from recent scRNA studies of SCN neurons for exploratory analysis [55,56].…”

Section: Resultssupporting

confidence: 63%

Gene expression plasticity of the mammalian brain circadian clock in response to photoperiod

Cox,

Gianonni-Guzmán,

Cartailler

et al. 2024

Preprint

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“…Captivity in toads from range‐core areas triggered molecular changes related to behaviour (GO:0008344 and GO:0007612), lipid and carbohydrate metabolism (GO:0009103 and GO:0016051), the immune system (GO:0002481, GO:0002485, GO:0002489 and GO:0002591), transcription (GO:0006351, GO:0006355 and GO:0045893), the response to stimulus (GO:0007186), and the response to stress (GO:0006950, GO:0009409, GO:0009408 and GO:0046677). Changes in expression levels in genes related to transcription have been documented in several studies investigating the transcriptomic consequences of environmental fluctuations, for example, in tambaquis ( Colossoma macropomum ) after a change in thermal conditions (Fé‐Gonçalves, Araújo, Santos, & Almeida‐Val, 2020 ), or during winter torpor in Djungarian hamsters ( Phodopus sungorus ) (Haugg et al, 2021 ). Captivity thus appeared to have affected similar molecular pathways in range‐core toads.…”

Section: Discussionmentioning

confidence: 99%

Captivity induces large and population‐dependent brain transcriptomic changes in wild‐caught cane toads (Rhinella marina)

et al. 2022

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Gene expression levels are key molecular phenotypes at the interplay between genotype and environment. Mounting evidence suggests that short-term changes in environmental conditions, such as those encountered in captivity, can substantially affect gene expression levels. Yet, the exact magnitude of this effect, how general it is, and whether it results in parallel changes across populations are not well understood.Here, we take advantage of the well-studied cane toad, Rhinella marina, to examine the effect of short-term captivity on brain gene expression levels, and determine whether effects of captivity differ between long-colonized and vanguard populations of the cane toad's Australian invasion range. We compared the transcriptomes of wild-caught toads immediately assayed with those from toads captured from the same populations but maintained in captivity for seven months. We found large differences in gene expression levels between captive and wild-caught toads from the same population, with an over-representation of processes related to behaviour and the response to stress. Captivity had a much larger effect on both gene expression levels and gene expression variability in toads from vanguard populations compared to toads from long-colonized areas, potentially indicating an increased plasticity in toads at the leading edge of the invasion. Overall, our findings indicate that shortterm captivity can induce large and population-specific transcriptomic changes, which has significant implications for studies comparing phenotypic traits of wild-caught organisms from different populations that have been held in captivity.

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“…In the hypothalamus of the 13‐lined ground squirrel ( I. tridecemlineatus ), the proportion of increased to decreased DEGs was 6 : 4 in torpor entry and 7 : 3 in torpor arousal, each compared with IBA, but 2 : 8 in the within‐torpor comparison (torpor entry vs late torpor) [31]. Similar ratios of increased and decreased DEGs have been found in different heterotherms [28,29,31,34,57]. Transcriptional and translational processes are highly temperature sensitive [57–60].…”

Section: Discussionmentioning

confidence: 93%

“…Data basis is ET (n = 4), LT (n = 3), and IBA (n = 4). Those indicator genes differentially expressed with Padj < 0.05 out of a previously defined list with 68 genes[29]. The color code indicates decreased genes with log 2 (FC) < 0 (yellow), increased genes with log 2 (FC) > 0 (green), and genes differentially expressed in two of the three pairwise comparisons ET vs IBA, ET vs LT, and LT vs IBA (red).…”

mentioning

confidence: 99%

Comparative transcriptomics of the garden dormouse hypothalamus during hibernation

Haugg,

Borner,

Stalder

et al. 2023

FEBS Open Bio

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Torpor or heterothermy is an energy saving mechanism used by endotherms to overcome harsh environmental conditions. During winter, the garden dormouse (Eliomys quercinus) hibernates with multiday torpor bouts and body temperatures of a few degrees Celsius, interrupted by brief euthermic phases. This study investigates gene expression within the hypothalamus, the key brain area controlling energy balance, adding information on differential gene expression potentially relevant to orchestrate torpor. A de novo assembled transcriptome of the hypothalamus was generated from garden dormice hibernating under constant darkness without food and water at 5 °C. Samples were collected during early torpor, late torpor, and interbout arousal. During early torpor, 765 genes were differentially expressed as compared with interbout arousal. Twenty‐seven pathways were over‐represented, including pathways related to hemostasis, extracellular matrix organization and signaling of small molecules. Only 82 genes were found to be differentially expressed between early and late torpor, and no pathways were over‐represented. During late torpor, 924 genes were differentially expressed relative to interbout arousal. Despite the high number of differentially expressed genes, only 10 pathways were over‐represented. Of these, eight were also observed to be over‐represented when comparing early torpor and interbout arousal. Our results are largely consistent with previous findings in other heterotherms. The addition of a transcriptome of a novel species may help to identify species‐specific and overarching torpor mechanisms through future species comparisons.

show abstract

Comparative transcriptomics of the Djungarian hamster hypothalamus during short photoperiod acclimation and spontaneous torpor

Cited by 10 publications

References 101 publications

Gene expression plasticity of the mammalian brain circadian clock in response to photoperiod

Gene expression plasticity of the mammalian brain circadian clock in response to photoperiod

Captivity induces large and population‐dependent brain transcriptomic changes in wild‐caught cane toads (Rhinella marina)

Comparative transcriptomics of the garden dormouse hypothalamus during hibernation

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