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Nocturnin expression is induced by fasting in the white adipose tissue of restricted fed mice.

Gilbert MR, Douris N, Tongjai S, Green CB - PLoS ONE (2011)

Bottom Line: The relationship between circadian clocks and metabolism is intimate and complex and a number of recent studies have begun to reveal previously unknown effects of food and its temporal availability on the clock and the rhythmic transcriptome of peripheral tissues.A rise in cAMP levels also induces Nocturnin expression, suggesting that Nocturnin's induction in eWAT by fasting is likely mediated through the same pathways that activate lipolysis.Therefore, this suggests that Nocturnin plays a role in linking nutrient sensing by the circadian clock to lipid mobilization in the adipocytes.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Virginia, Charlottesville, Virginia, United States of America.

ABSTRACT
The relationship between circadian clocks and metabolism is intimate and complex and a number of recent studies have begun to reveal previously unknown effects of food and its temporal availability on the clock and the rhythmic transcriptome of peripheral tissues. Nocturnin, a circadian deadenylase, is expressed rhythmically in a wide variety of tissues, but we report here that Nocturnin expression is arrhythmic in epididymal white adipose tissue (eWAT) of mice housed in 12:12 LD with ad libitum access to food. However, Nocturnin expression becomes rhythmic in eWAT of mice placed on restricted feeding. We show here that Nocturnin's rhythmic expression pattern is not dependent upon feeding, nor is it acutely induced by feeding in the liver or eWAT of ad libitum fed mice. However, Nocturnin is acutely induced by the absence of the expected meal in eWAT of restricted fed mice. A rise in cAMP levels also induces Nocturnin expression, suggesting that Nocturnin's induction in eWAT by fasting is likely mediated through the same pathways that activate lipolysis. Therefore, this suggests that Nocturnin plays a role in linking nutrient sensing by the circadian clock to lipid mobilization in the adipocytes.

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Related in: MedlinePlus

Nocturnin expression is not dependent upon or induced by feeding.(A) Nocturnin expression is not dependent upon feeding. The top panel is a schematic depicting the experimental setup. Open bars represent lights on, and the closed bars represent lights off. The dotted line depicts food availability. Graphs (left) represent the mean relative mRNA level (±SEM) for each time point in liver (top) and eWAT (bottom), n = 3–6. CircWave analysis (right panels of A) shows the corresponding statistical analyses for rhythmicity. In the CircWave graphs, each dot represents the normalized relative mRNA level from the eWAT of an individual mouse. The curve represents the best-fit fourier curve, with the center of gravity (phase) represented by the vertical bar intersecting with the horizontal bar which represents the mean of the entire data set (liver; p≤0.002). Data set for which a fourier curve could not be fitted (eWAT) is indicated by ‡. (B) Nocturnin expression is not induced by fasting. Schematic of fasting experiment (top panel) as described in (A). The bar with vertical stripes represents the fasting period. Graphs represent the mean (±SEM) for each group, n = 4. (C) Nocturnin expression is not induced by feeding after a fast. Schematic representation of experiment is as described in (A) and (B). The solid black bar in the “refed” condition represents the time period in which food was made available after the fast. Gene expression analysis of the liver (middle panel) and eWAT (bottom panel) collected at ZT4 shows that Nocturnin is not induced by feeding after a fast, though the expected changes in expression patterns of Srebp-1c and Pgc-1α were observed (see text). Data represent the mean (±SEM), n = 3 for each group.
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pone-0017051-g001: Nocturnin expression is not dependent upon or induced by feeding.(A) Nocturnin expression is not dependent upon feeding. The top panel is a schematic depicting the experimental setup. Open bars represent lights on, and the closed bars represent lights off. The dotted line depicts food availability. Graphs (left) represent the mean relative mRNA level (±SEM) for each time point in liver (top) and eWAT (bottom), n = 3–6. CircWave analysis (right panels of A) shows the corresponding statistical analyses for rhythmicity. In the CircWave graphs, each dot represents the normalized relative mRNA level from the eWAT of an individual mouse. The curve represents the best-fit fourier curve, with the center of gravity (phase) represented by the vertical bar intersecting with the horizontal bar which represents the mean of the entire data set (liver; p≤0.002). Data set for which a fourier curve could not be fitted (eWAT) is indicated by ‡. (B) Nocturnin expression is not induced by fasting. Schematic of fasting experiment (top panel) as described in (A). The bar with vertical stripes represents the fasting period. Graphs represent the mean (±SEM) for each group, n = 4. (C) Nocturnin expression is not induced by feeding after a fast. Schematic representation of experiment is as described in (A) and (B). The solid black bar in the “refed” condition represents the time period in which food was made available after the fast. Gene expression analysis of the liver (middle panel) and eWAT (bottom panel) collected at ZT4 shows that Nocturnin is not induced by feeding after a fast, though the expected changes in expression patterns of Srebp-1c and Pgc-1α were observed (see text). Data represent the mean (±SEM), n = 3 for each group.

Mentions: The fact that Nocturnin was acutely induced by stimuli such as TPA and insulin in vitro raised the possibility that Nocturnin may be acutely induced in response to feeding [14], [15]. Nocturnin expression peaks in the early night in the livers of ad libitum fed mice housed in 12∶12 light:dark (LD) conditions (Figure 1A; [12], [13]). However, quantitative real-time PCR analysis of the epididymal white adipose tissue (eWAT) from ad libitum fed mice housed in 12∶12 light:dark revealed that Nocturnin is expressed at low levels, and is statistically arrhythmic (Figure 1A, bottom panel). Nocturnin expression is arrhythmic despite rhythmic core clock gene expression in eWAT [20], [21]. The observation that Nocturnin's expression pattern can be driven by systemic cues in the liver with a peak expression in the early night [16] led us to hypothesize that this expression pattern could be the result of an acute induction of Nocturnin caused by the large bout of feeding which begins at the onset of darkness [22]. To test this, mice were habituated to a 12∶12 LD cycle and then fasted for 25 hours, beginning at ZT12 (ZT refers to “zeitgeber time” in hours, where ZT0 is light onset and ZT12 is light offset) and ending at ZT13 the next day (Figure 1B, top panel). Contrary to our hypothesis, we found that Nocturnin expression both in the liver and in the white adipose tissue was not dependent upon the presence of food (Figure 1B, bottom panel).


Nocturnin expression is induced by fasting in the white adipose tissue of restricted fed mice.

Gilbert MR, Douris N, Tongjai S, Green CB - PLoS ONE (2011)

Nocturnin expression is not dependent upon or induced by feeding.(A) Nocturnin expression is not dependent upon feeding. The top panel is a schematic depicting the experimental setup. Open bars represent lights on, and the closed bars represent lights off. The dotted line depicts food availability. Graphs (left) represent the mean relative mRNA level (±SEM) for each time point in liver (top) and eWAT (bottom), n = 3–6. CircWave analysis (right panels of A) shows the corresponding statistical analyses for rhythmicity. In the CircWave graphs, each dot represents the normalized relative mRNA level from the eWAT of an individual mouse. The curve represents the best-fit fourier curve, with the center of gravity (phase) represented by the vertical bar intersecting with the horizontal bar which represents the mean of the entire data set (liver; p≤0.002). Data set for which a fourier curve could not be fitted (eWAT) is indicated by ‡. (B) Nocturnin expression is not induced by fasting. Schematic of fasting experiment (top panel) as described in (A). The bar with vertical stripes represents the fasting period. Graphs represent the mean (±SEM) for each group, n = 4. (C) Nocturnin expression is not induced by feeding after a fast. Schematic representation of experiment is as described in (A) and (B). The solid black bar in the “refed” condition represents the time period in which food was made available after the fast. Gene expression analysis of the liver (middle panel) and eWAT (bottom panel) collected at ZT4 shows that Nocturnin is not induced by feeding after a fast, though the expected changes in expression patterns of Srebp-1c and Pgc-1α were observed (see text). Data represent the mean (±SEM), n = 3 for each group.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3037405&req=5

pone-0017051-g001: Nocturnin expression is not dependent upon or induced by feeding.(A) Nocturnin expression is not dependent upon feeding. The top panel is a schematic depicting the experimental setup. Open bars represent lights on, and the closed bars represent lights off. The dotted line depicts food availability. Graphs (left) represent the mean relative mRNA level (±SEM) for each time point in liver (top) and eWAT (bottom), n = 3–6. CircWave analysis (right panels of A) shows the corresponding statistical analyses for rhythmicity. In the CircWave graphs, each dot represents the normalized relative mRNA level from the eWAT of an individual mouse. The curve represents the best-fit fourier curve, with the center of gravity (phase) represented by the vertical bar intersecting with the horizontal bar which represents the mean of the entire data set (liver; p≤0.002). Data set for which a fourier curve could not be fitted (eWAT) is indicated by ‡. (B) Nocturnin expression is not induced by fasting. Schematic of fasting experiment (top panel) as described in (A). The bar with vertical stripes represents the fasting period. Graphs represent the mean (±SEM) for each group, n = 4. (C) Nocturnin expression is not induced by feeding after a fast. Schematic representation of experiment is as described in (A) and (B). The solid black bar in the “refed” condition represents the time period in which food was made available after the fast. Gene expression analysis of the liver (middle panel) and eWAT (bottom panel) collected at ZT4 shows that Nocturnin is not induced by feeding after a fast, though the expected changes in expression patterns of Srebp-1c and Pgc-1α were observed (see text). Data represent the mean (±SEM), n = 3 for each group.
Mentions: The fact that Nocturnin was acutely induced by stimuli such as TPA and insulin in vitro raised the possibility that Nocturnin may be acutely induced in response to feeding [14], [15]. Nocturnin expression peaks in the early night in the livers of ad libitum fed mice housed in 12∶12 light:dark (LD) conditions (Figure 1A; [12], [13]). However, quantitative real-time PCR analysis of the epididymal white adipose tissue (eWAT) from ad libitum fed mice housed in 12∶12 light:dark revealed that Nocturnin is expressed at low levels, and is statistically arrhythmic (Figure 1A, bottom panel). Nocturnin expression is arrhythmic despite rhythmic core clock gene expression in eWAT [20], [21]. The observation that Nocturnin's expression pattern can be driven by systemic cues in the liver with a peak expression in the early night [16] led us to hypothesize that this expression pattern could be the result of an acute induction of Nocturnin caused by the large bout of feeding which begins at the onset of darkness [22]. To test this, mice were habituated to a 12∶12 LD cycle and then fasted for 25 hours, beginning at ZT12 (ZT refers to “zeitgeber time” in hours, where ZT0 is light onset and ZT12 is light offset) and ending at ZT13 the next day (Figure 1B, top panel). Contrary to our hypothesis, we found that Nocturnin expression both in the liver and in the white adipose tissue was not dependent upon the presence of food (Figure 1B, bottom panel).

Bottom Line: The relationship between circadian clocks and metabolism is intimate and complex and a number of recent studies have begun to reveal previously unknown effects of food and its temporal availability on the clock and the rhythmic transcriptome of peripheral tissues.A rise in cAMP levels also induces Nocturnin expression, suggesting that Nocturnin's induction in eWAT by fasting is likely mediated through the same pathways that activate lipolysis.Therefore, this suggests that Nocturnin plays a role in linking nutrient sensing by the circadian clock to lipid mobilization in the adipocytes.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Virginia, Charlottesville, Virginia, United States of America.

ABSTRACT
The relationship between circadian clocks and metabolism is intimate and complex and a number of recent studies have begun to reveal previously unknown effects of food and its temporal availability on the clock and the rhythmic transcriptome of peripheral tissues. Nocturnin, a circadian deadenylase, is expressed rhythmically in a wide variety of tissues, but we report here that Nocturnin expression is arrhythmic in epididymal white adipose tissue (eWAT) of mice housed in 12:12 LD with ad libitum access to food. However, Nocturnin expression becomes rhythmic in eWAT of mice placed on restricted feeding. We show here that Nocturnin's rhythmic expression pattern is not dependent upon feeding, nor is it acutely induced by feeding in the liver or eWAT of ad libitum fed mice. However, Nocturnin is acutely induced by the absence of the expected meal in eWAT of restricted fed mice. A rise in cAMP levels also induces Nocturnin expression, suggesting that Nocturnin's induction in eWAT by fasting is likely mediated through the same pathways that activate lipolysis. Therefore, this suggests that Nocturnin plays a role in linking nutrient sensing by the circadian clock to lipid mobilization in the adipocytes.

Show MeSH
Related in: MedlinePlus