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. 2016 Apr 19;6:24627.
doi: 10.1038/srep24627.

The Hibernating South American Marsupial, Dromiciops Gliroides, Displays Torpor-Sensitive microRNA Expression Patterns

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Free PMC article

The Hibernating South American Marsupial, Dromiciops Gliroides, Displays Torpor-Sensitive microRNA Expression Patterns

Hanane Hadj-Moussa et al. Sci Rep. .
Free PMC article

Abstract

When faced with adverse environmental conditions, the marsupial Dromiciops gliroides uses either daily or seasonal torpor to support survival and is the only known hibernating mammal in South America. As the sole living representative of the ancient Order Microbiotheria, this species can provide crucial information about the evolutionary origins and biochemical mechanisms of hibernation. Hibernation is a complex energy-saving strategy that involves changes in gene expression that are elicited in part by microRNAs. To better elucidate the role of microRNAs in orchestrating hypometabolism, a modified stem-loop technique and quantitative PCR were used to characterize the relative expression levels of 85 microRNAs in liver and skeletal muscle of control and torpid D. gliroides. Thirty-nine microRNAs were differentially regulated during torpor; of these, 35 were downregulated in liver and 11 were differentially expressed in skeletal muscle. Bioinformatic analysis predicted that the downregulated liver microRNAs were associated with activation of MAPK, PI3K-Akt and mTOR pathways, suggesting their importance in facilitating marsupial torpor. In skeletal muscle, hibernation-responsive microRNAs were predicted to regulate focal adhesion, ErbB, and mTOR pathways, indicating a promotion of muscle maintenance mechanisms. These tissue-specific responses suggest that microRNAs regulate key molecular pathways that facilitate hibernation, thermoregulation, and prevention of muscle disuse atrophy.

Figures

Figure 1
Figure 1. Heat map showing torpor-induced changes in the relative expression of 35 miRNAs in liver and 11 miRNAs in skeletal muscle of the marsupial D. gliroides.
MicroRNA relative expression was evaluated by RT-qPCR of reverse-transcribed, polyadenylated transcripts. Data represent means of n = 4 biological replicates from different animals. Relative expression of genes was calculated by standardizing against U6 snRNA expression. Control values were adjusted to 1 and the torpid values were expressed relative to the controls. The reported miRNA expression level changes in torpid individuals were all statistically significant from the corresponding control; statistical testing used the Student’s t-test where p < 0.05. The legend provides a visual reference for the colour gradient used. Different shades of red represent significant downregulation of miRNA in the torpid state versus control; increasing redness signifies greater relative downregulation during torpor. Black represents no significant changes. Increasing greenness represents greater upregulation of miRNA during torpor versus control. For the relative expression ± SEM values of all 85 miRNA species examined refer to Supplementary Table S2.
Figure 2
Figure 2. DIANA mirPath analysis of 35 torpor-repressed miRNAs in D. gliroides liver predicted that 32 genes involved in mTOR signalling are targeted by 23 miRNAs from this group.
This figure illustrates which genes are predicted to be upregulated during torpor (grey boxes) and their putative miRNA regulators (red bars indicate decreased miRNA expression during torpor) within the context of a simplified Akt/mTOR signalling pathway. Genes in white boxes were not predicted targets of the 35 suppressed miRNAs in liver.
Figure 3
Figure 3. DIANA mirPath analysis of eleven miRNAs showing torpor-specific expression in D. gliroides skeletal muscle predicted that twelve genes involved in mTOR signalling are targeted by eight miRNAs from this group.
Predicted target genes (grey boxes) and their putative miRNA regulators (green bars indicate increased miRNA expression and red bars indicate decreased miRNA expression during torpor) are shown in the context of a simplified Akt/mTOR signalling pathway. Genes in white boxes were not predicted targets of the eleven differentially expressed miRNAs in skeletal muscle.

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