Quantitative ultrastructural changes of hepatocyte constituents in euthermic, hibernating and arousing dormice (Muscardinus avellanarius)

Malatesta, Manuela; Zancanaro, Carlo; Baldelli, B.; Gazzanelli, Giancarlo

doi:10.1016/s0040816602000745

Cited by 16 publications

(16 citation statements)

References 20 publications

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“…Malatesta et al (2002) found that the total cell and cytoplasm area of hepatocytes from hibernating dormice (Muscardinus avellanarius) was significantly reduced compared with those from euthermic dormice. High energy phosphates are maintained in hibernation; decreases in actin-ATP hydrolysis and turnover may contribute to energy conservation and changes in cell size (Lust et al, 1989;Storey, 1997;Bernstein and Bamburg, 2003).…”

Section: Discussionmentioning

confidence: 95%

“…High energy phosphates are maintained in hibernation; decreases in actin-ATP hydrolysis and turnover may contribute to energy conservation and changes in cell size (Lust et al, 1989;Storey, 1997;Bernstein and Bamburg, 2003). Malatesta et al (2002) suggested that the change in cell structure was related to marked reduction in hepatocyte function found in the hibernating dormouse. Whether similar mechanisms are involved in neuronal cell size changes in AGS remains to be elucidated.…”

Section: Discussionmentioning

confidence: 99%

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Distribution of NMDA receptor subunit NR1 in Arctic ground squirrel central nervous system

Zhao

Christian

Castillo

et al. 2006

Journal of Chemical Neuroanatomy

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Hibernation is a natural model of neuroprotection and adult synaptic plasticity. NMDA receptors (NMDAR), which play key roles in excitotoxicity and synaptic plasticity, have not been characterized in a hibernating species. Tolerance to excitotoxicity and cognitive enhancement in Arctic ground squirrels (AGS, Spermophilus parryii) suggests that NMDAR expression may decrease in hibernation and increase upon arousal. NMDAR consist of at least one NMDAR1 (NR1) subunit, which is required for receptor function. Localization of NR1 reflects localization of the majority, if not all, NMDAR complexes. The purpose of this study, therefore, was to characterize the distribution of NR1 subunits in AGS central nervous system using immunohistochemistry. In addition, we compare NR1 expression in hippocampus of hibernating AGS (hAGS) and inter-bout euthermic AGS (ibeAGS) and assess changes in cell somata size using NR1 stained sections in three hippocampal sub-regions (CA1, CA3, and dentate gyrus). For the first time, we report that immunoreactivity of anti-NR1 is widely distributed throughout the central nervous system in AGS and is similar to other species. No differences exist in the expression and distribution of NR1 in hAGS and ibeAGS. However, we report a significant decrease in size of hippocampal CA1 and dentate gyrus NR1-expressing neuronal somata during hibernation torpor.

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Section: Discussionmentioning

confidence: 95%

Section: Discussionmentioning

confidence: 99%

Distribution of NMDA receptor subunit NR1 in Arctic ground squirrel central nervous system

Zhao

Christian

Castillo

et al. 2006

Journal of Chemical Neuroanatomy

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“…Concentrations of glucose in plasma decrease by about one-half (from 10 to 5 mM) within the first day of torpor in AGS (43), and although gluconeogenesis replenishes some glycogen stores during arousal (17), glycogen pools are largely depleted (35). Moreover, the activity of glycogen synthase is decreased during hibernation (21).…”

Section: Discussionmentioning

confidence: 99%

Absence of cellular stress in brain after hypoxia induced by arousal from hibernation in Arctic ground squirrels

Liu

Zhu²,

Rivera

et al. 2005

American Journal of Physiology-Regulatory, Integrative and Comp

119

133

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Although hypoxia tolerance in heterothermic mammals is well established, it is unclear whether the adaptive significance stems from hypoxia or other cellular challenge associated with euthermy, hibernation, or arousal. In the present study, blood gases, hemoglobin O 2 saturation (SO2), and indexes of cellular and physiological stress were measured during hibernation and euthermy and after arousal thermogenesis. Results show that arterial O 2 tension (PaO 2 ) and SO2 are severely diminished during arousal and that hypoxia-inducible factor (HIF)-1␣ accumulates in brain. Despite evidence of hypoxia, neither cellular nor oxidative stress, as indicated by inducible nitric oxide synthase (iNOS) levels and oxidative modification of biomolecules, was observed during late arousal from hibernation. Compared with rats, hibernating Arctic ground squirrels (Spermophilus parryii) are well oxygenated with no evidence of cellular stress, inflammatory response, neuronal pathology, or oxidative modification following the period of high metabolic demand necessary for arousal. In contrast, euthermic Arctic ground squirrels experience mild, chronic hypoxia with low SO 2 and accumulation of HIF-1␣ and iNOS and demonstrate the greatest degree of cellular stress in brain. These results suggest that Arctic ground squirrels experience and tolerate endogenous hypoxia during euthermy and arousal.torpor; ischemia; stroke; Spermophilus parryii; reperfusion; inflammation; oxidative stress HIBERNATION IS A UNIQUE PHYSIOLOGICAL STATE of prolonged periods of low body temperature, metabolism, blood flow, and other physiological processes that are disrupted by brief periodic arousal episodes when animals rewarm and reperfuse metabolically active tissues (7). During arousal thermogenesis, blood flow returns to brain and other organs in a reperfusionlike manner at a time of maximal oxygen demand (42, 58). Preservation of neuronal and other cellular morphology during low cerebral blood flow demonstrates that hibernating mammals tolerate pronounced fluctuations in blood flow (16,61). Physiological and cellular stress experienced during euthermy, hibernation, and arousal is less well characterized.Arterial oxygen tension (Pa O 2 ) and tissue lactate measurements show that hibernating ground squirrels are well oxygenated (16,20), sometimes exceeding values in the euthermic state (15). In contrast, oxygen supply may become limiting during arousal thermogenesis. Increases in brain tissue lactate levels during peak oxygen consumption during arousal from hibernation in bats suggest these animals experience oxygen deficiency during arousal and reperfusion (30). However, because tissue lactate was not reported for euthermic bats, it is unclear how brain tissue hypoxia experienced during arousal compares to the euthermic state. Moreover, Pa O 2 was not measured to address the relationship between blood and tissue oxygenation during euthermy, hibernation, and arousal. To characterize physiological challenges associated with arousal thermogenesis, we evaluated b...

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“…Structural reorganization also occurs in the cytoplasm during hibernation. Electron microscopy has shown that liver structures associated with protein synthesis (rough endoplasmic reticulum) and post-translational processing (Golgi complex) also degrade during hibernation in dormice but reform again upon arousal (Malatesta et al, 2002). 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.…”

Section: Reviewmentioning

confidence: 99%

Regulation of hypometabolism: insights into epigenetic controls

Storey

2015

Journal of Experimental Biology

145

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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Quantitative ultrastructural changes of hepatocyte constituents in euthermic, hibernating and arousing dormice (Muscardinus avellanarius)

Cited by 16 publications

References 20 publications

Distribution of NMDA receptor subunit NR1 in Arctic ground squirrel central nervous system

Distribution of NMDA receptor subunit NR1 in Arctic ground squirrel central nervous system

Absence of cellular stress in brain after hypoxia induced by arousal from hibernation in Arctic ground squirrels

Regulation of hypometabolism: insights into epigenetic controls

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