Abstract
Animals living at high or temperate latitudes are challenged by extensive changes in environmental conditions over seasons. Djungarian hamsters (Phodopus sungorus) are able to cope with extremely cold ambient temperatures and food scarcity in winter by expressing spontaneous daily torpor. Daily torpor is a circadian controlled voluntary reduction of metabolism that can reduce energy expenditure by up to 65% when used frequently. In the past decades it has become more and more apparent, that the hypothalamus is likely to play a key role in regulating induction and maintenance of daily torpor, but the molecular signals, which lead to the initiation of daily torpor, are still unknown. Here we present the first transcriptomic study of hypothalamic gene expression patterns in Djungarian hamsters during torpor entrance. Based on Illumina sequencing we were able to identify a total number of 284 differentially expressed genes, whereby 181 genes were up- and 103 genes down regulated during torpor entrance. The 20 most up regulated group contained eight genes coding for structure proteins, including five collagen genes, dnha2 and myo15a, as well as the procoagulation factor vwf. In a proximate approach we investigated these genes by quantitative real-time PCR (qPCR) analysis over the circadian cycle in torpid and normothermic animals at times of torpor entrance, mid torpor, arousal and post-torpor. These qPCR data confirmed up regulation of dnah2, myo15a, and vwf during torpor entrance, but a decreased mRNA level for all other investigated time points. This suggests that gene expression of structure genes as well as the procoagulation factor are specifically initiated during the early state of torpor and provides evidence for protective molecular adaptions in the hypothalamus of Djungarian hamsters including changes in structure, transport of biomolecules and coagulation.
Highlights
Metabolic depression is a commonly used strategy of mammals to survive winter
Whether differential candidate gene expression is restricted to torpor entrance and to assess circadian regulation, we investigated relative mRNA expression at Zeitgebertime 1 (ZT1), ZT4, ZT7, and ZT16 in animals undergoing torpor and animals remaining normothermic
Our data show 284 differentially expressed genes out of 27,830 identified genes in the hypothalamus of P. sungorus during entrance into the torpid state, implying that just a small set of genes is affected by the metabolic depression initiating torpor entrance
Summary
Metabolic depression (torpor) is a commonly used strategy of mammals to survive winter. The Djungarian hamster ( known as Siberian hamster, P. sungorus) has evolved a number of physiological and morphological adaptations (e.g., voluntary reduction of body weight, molt to dense white winter coat, gonadal regression, torpor) to seasonally reduce energy requirements (Figala et al, 1973; Scherbarth and Steinlechner, 2010). The most effective adaptive trait is the expression of daily torpor that spontaneously occurs after 10– 12 weeks in short days once all other physiological adaptations are completed and the corresponding hormonal systems are in winter state (reduced levels of prolactin, testosterone and leptin) (Cubuk et al, 2016). Torpor is initiated by an active depression of metabolic rate (25% below the level of resting metabolic rate), accompanied by reduced heart rate and ventilation as well as a decrease in body temperature (Tb) to > 15◦C and reduced physical locomotor activity (Heldmaier and Ruf, 1992; Heldmaier et al, 2004). The incidence of daily torpor is highly variable between individuals as well as in the same animal (1–7 torpor bouts per week) and can save up to 65% of total energy requirements, when torpor is used on a daily basis (Heldmaier, 1981; Kirsch et al, 1991; Ruf et al, 1991)
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