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The hibernating South American marsupial, Dromiciops gliroides, displays torpor-sensitive microRNA expression patterns.

Hadj-Moussa H, Moggridge JA, Luu BE, Quintero-Galvis JF, Gaitán-Espitia JD, Nespolo RF, Storey KB - Sci Rep (2016)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology and Institute of Biochemistry, Carleton University, 1125 Colonel By Drive, Ottawa, Ontario K1S 5B6, Canada.

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.

No MeSH data available.


Related in: MedlinePlus

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.
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f1: 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.

Mentions: The primary goal of this study was to characterize hibernation-specific patterns of miRNA expression in liver and skeletal muscle of the marsupial D. gliroides. Of the 85 miRNAs successfully quantified by RT-qPCR, 35 miRNAs were significantly down-regulated in liver during torpor, with miRNA relative abundances decreasing by 0.21–0.72 fold change from the control condition (p < 0.05; Supplementary Table S2 and Fig. 1). A different pattern was observed in skeletal muscle, where seven miRNAs showed elevated expression during torpor, increasing by 0.32–1.52 fold change from control levels (dgl-miR-1a-1-5p, dgl-miR-1b-5p, dgl-miR-139-5p, dgl-miR-181a-3p, dgl-miR-190a-5p, dgl-miR-483-5p, and dgl-miR-99b-5p), whereas, 4 miRNAs showed decreased expression of 0.33-0.43 fold change compared to control (dgl-miR-16-1-3p, dgl-miR-185-5p, dgl-miR-22-5p, and dgl-miR-33a-5p) (p < 0.05; Supplementary Table S2 and Fig. 1). Of these, three miRNAs showed a pattern of decreased expression that was consistent in both tissues during torpor (dgl-miR-16-3p, dgl-miR-22-5p, and dgl-miR-185-5p). In contrast, four miRNAs (dgl-miR-1a1-5p, dgl-miR-1b-5p, dgl-miR-99b-5p, and dgl-miR-139-5p) showed a torpor-specific increase in skeletal muscle, but with a concomitant decrease in liver tissue.


The hibernating South American marsupial, Dromiciops gliroides, displays torpor-sensitive microRNA expression patterns.

Hadj-Moussa H, Moggridge JA, Luu BE, Quintero-Galvis JF, Gaitán-Espitia JD, Nespolo RF, Storey KB - Sci Rep (2016)

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.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4835794&req=5

f1: 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.
Mentions: The primary goal of this study was to characterize hibernation-specific patterns of miRNA expression in liver and skeletal muscle of the marsupial D. gliroides. Of the 85 miRNAs successfully quantified by RT-qPCR, 35 miRNAs were significantly down-regulated in liver during torpor, with miRNA relative abundances decreasing by 0.21–0.72 fold change from the control condition (p < 0.05; Supplementary Table S2 and Fig. 1). A different pattern was observed in skeletal muscle, where seven miRNAs showed elevated expression during torpor, increasing by 0.32–1.52 fold change from control levels (dgl-miR-1a-1-5p, dgl-miR-1b-5p, dgl-miR-139-5p, dgl-miR-181a-3p, dgl-miR-190a-5p, dgl-miR-483-5p, and dgl-miR-99b-5p), whereas, 4 miRNAs showed decreased expression of 0.33-0.43 fold change compared to control (dgl-miR-16-1-3p, dgl-miR-185-5p, dgl-miR-22-5p, and dgl-miR-33a-5p) (p < 0.05; Supplementary Table S2 and Fig. 1). Of these, three miRNAs showed a pattern of decreased expression that was consistent in both tissues during torpor (dgl-miR-16-3p, dgl-miR-22-5p, and dgl-miR-185-5p). In contrast, four miRNAs (dgl-miR-1a1-5p, dgl-miR-1b-5p, dgl-miR-99b-5p, and dgl-miR-139-5p) showed a torpor-specific increase in skeletal muscle, but with a concomitant decrease in liver tissue.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology and Institute of Biochemistry, Carleton University, 1125 Colonel By Drive, Ottawa, Ontario K1S 5B6, Canada.

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.

No MeSH data available.


Related in: MedlinePlus