Hepatic polyribosomes and protein synthesis: Seasonal changes in a hibernator

Whitten, Bertwell K.; Schrader, L. E.; Huston, R. L.; Honold, Guy R.

doi:10.1016/0020-711x(70)90053-4

Cited by 16 publications

(8 citation statements)

References 8 publications

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“…These findings agree with previous work demonstrating a disaggregation of polysomes in torpid ground squirrels; moreover, extracts prepared from hibernating animals, when warmed and assayed at 37°C, still display an approximately threefold reduction in translation (13,37). Frerichs and coworkers further demonstrated in vivo that as an animal is entering torpor but is still at a relatively high body temperature (body temperature decreased from 19.0 to 7.5°C during a 2-h experiment), protein synthesis is still suppressed, as measured by [ 14 C]leucine administration (13).…”

Section: Discussionsupporting

confidence: 92%

“…During active protein synthesis, mRNAs are associated with multiple ribosomes, forming polysomes. During the hibernation of ground squirrels, there is a marked loss of polysomes in liver and brain (13,37). If arousal episodes allow protein synthesis to occur, thereby replenishing proteins depleted during torpor, then polysomes are expected to be depleted during torpor and then reappear during arousals.…”

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confidence: 99%

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mRNA Stability and Polysome Loss in Hibernating Arctic Ground Squirrels (Spermophilus parryii)

Knight

Narus

Martin

et al. 2000

Molecular and Cellular Biology

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All small mammalian hibernators periodically rewarm from torpor to high, euthermic body temperatures for brief intervals throughout the hibernating season. The functional significance of these arousal episodes is unknown, but one suggestion is that rewarming may be related to replacement of gene products lost during torpor due to degradation of mRNA. To assess the stability of mRNA as a function of the hibernation state, we examined the poly(A) tail lengths of liver mRNA from arctic ground squirrels sacrificed during four hibernation states (early and late during a torpor bout and early and late following arousal from torpor) and from active ground squirrels sacrificed in the summer. Poly(A) tail lengths were not altered during torpor, suggesting either that mRNA is stabilized or that transcription continues during torpor. In mRNA isolated from torpid ground squirrels, we observed a pattern of 12 poly(A) residues at greater densities approximately every 27 nucleotides along the poly(A) tail, which is a pattern consistent with binding of poly(A)-binding protein. The intensity of this pattern was significantly reduced following arousal from torpor and undetectable in mRNA obtained from summer ground squirrels. Analyses of polysome profiles revealed a significant reduction in polyribosomes in torpid animals, indicating that translation is depressed during torpor.Hibernation in mammals is an energy-conserving strategy involving physiological and behavioral accommodations to low body temperature and low metabolic rate for extended, but not indefinite, periods (12). Hibernation involves a cyclic up-and down-regulation of metabolism (36). The arctic ground squirrel (Spermophilus parryii) illustrates an extreme example of hibernation under adverse conditions.

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Section: Discussionsupporting

confidence: 92%

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confidence: 99%

mRNA Stability and Polysome Loss in Hibernating Arctic Ground Squirrels (Spermophilus parryii)

Knight

Narus

Martin

et al. 2000

Molecular and Cellular Biology

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“…The results (Table 2) do not fully resolve this question since the rates of protein synthesis in the pectoratis muscles of aroused bats are significantly lower than those of fasted summer bats, but the rates of hepatic protein synthesis do not differ between these groups ( Table 2). The high rates of hepatic protein synthesis observed in bats aroused from hibernation contrast sharply with earlier studies of hibernating ground squirrels (Spermophilus tridecemlineatus), which suggest that hepatic polyribosomes are deaggregated (Whitten et al 1970) and that cell-free preparations of livers have significantly lower protein synthetic capacities than do those of summer squirrels .…”

Section: Discussioncontrasting

confidence: 80%

Protein metabolism in the pectoralis muscle and liver of hibernating bats,Eptesicus fuscus

Yacoe

1983

J Comp Physiol B

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Summary. Seasonal variations in protein metabolism of the pectoralis muscle and liver of the big brown bat, Eptesicus fuscus, are examined in relation to seasonal changes in physiological status. A technique is described for the determination of protein synthetic rates in vivo in animals too small for conventional methods. The results indicate no detectable rates of protein synthesis in hibernating bats during torpor bouts ( Table 2). Rates of synthesis in hibernating bats during periods of arousal are comparable to those of active summer bats (Table 2), despite the fact that the hibernating bats had not eaten in over 2 months. Rates of protein degradation were calculated from the rate of urea formation in torpid bats (Figs. 4, 5), the overall loss of pectoralis muscle and liver protein mass during hibernation (Table 3), the proportion of the total time of hibernation spent in torpor and arousal (Table 1), and the observed rates of protein synthesis (Table 2). These estimates (Table 4) indicate negligible rates of protein degradation in torpid bats. However, protein degradation during periodic arousals is comparable to that of summer bats after an overnight fast. These findings are consistent with earlier observations suggesting that significant gluconeogenesis from tissue protein occurs during spontaneous arousals from hibernation.

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“…The authors proposed that this may be a fast and energetically efficient way to respond to a huge reduction in the demand for protein synthesis while still retaining the capacity to reactivate this ATP-expensive cell function immediately upon arousal. Multiple studies have documented polysome dissociation during mammalian hibernation (Whitten et al, 1970;Frerichs et al, 1998;Knight et al, 2000;Hittel and Storey, 2002) and other forms of hypometabolism (e.g. hypoxia, anoxia), with an opposite increase in monosomes and a sequestering of most mRNA transcripts into monosome and/or ribonuclear protein fractions (reviewed in Storey and Storey, 2004).…”

Section: Reviewmentioning

confidence: 99%

Regulation of hypometabolism: insights into epigenetic controls

Storey

2015

Journal of Experimental Biology

146

129

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For many animals, survival of severe environmental stress (e.g. to extremes of heat or cold, drought, oxygen limitation, food deprivation) is aided by entry into a hypometabolic state. Strong depression of metabolic rate, often to only 1-20% of normal resting rate, is a core survival strategy of multiple forms of hypometabolism across the animal kingdom, including hibernation, anaerobiosis, aestivation and freeze tolerance. Global biochemical controls are needed to suppress and reprioritize energy use; one such well-studied control is reversible protein phosphorylation. Recently, we turned our attention to the idea that mechanisms previously associated mainly with epigenetic regulation can also contribute to reversible suppression of gene expression in hypometabolic states. Indeed, situations as diverse as mammalian hibernation and turtle anoxia tolerance show coordinated changes in histone post-translational modifications (acetylation, phosphorylation) and activities of histone deacetylases, consistent with their use as mechanisms for suppressing gene expression during hypometabolism. Other potential mechanisms of gene silencing in hypometabolic states include altered expression of miRNAs that can provide post-transcriptional suppression of mRNA translation and the formation of ribonuclear protein bodies in the nucleus and cytoplasm to allow storage of mRNA transcripts until animals rouse themselves again. Furthermore, mechanisms first identified in epigenetic regulation (e.g. protein acetylation) are now proving to apply to many central metabolic enzymes (e.g. lactate dehydrogenase), suggesting a new layer of regulatory control that can contribute to coordinating the depression of metabolic rate.

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Hepatic polyribosomes and protein synthesis: Seasonal changes in a hibernator

Cited by 16 publications

References 8 publications

mRNA Stability and Polysome Loss in Hibernating Arctic Ground Squirrels (Spermophilus parryii)

mRNA Stability and Polysome Loss in Hibernating Arctic Ground Squirrels (Spermophilus parryii)

Protein metabolism in the pectoralis muscle and liver of hibernating bats,Eptesicus fuscus

Regulation of hypometabolism: insights into epigenetic controls

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