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PubMed1997

Protein kinase C from bat brain: the enzyme from a hibernating mammal.

Protein kinase C (PKC) from brain of euthermic and hibernating bats (Myotis lucifugus) showed only one form as determined by hydroxylapatite chromatography, compared with three forms found in rat brain. Cross-reaction with antibodies to rabbit alpha, beta, and gamma isozymes showed that bat brain contained only PKC(gamma). During hibernation the activity of PKC in bat brain decreased to 63% of the euthermic value but the percentage that was membrane-associated did not change. Bat and rat brain PKC(gamma) were purified to homogeneity. Both enzymes phosphorylated all three of the substrates tested (FKKSFKL-NH2 peptide substrate, histone H1, protamine), the bat enzyme having significantly higher K(m) values than rat PKC for both peptide and histone. Both enzymes required phospholipids and Ca2+ for activation with rat brain PKC depending almost exclusively on phosphatidylserine. Bat PKC, however, made use of other phospholipids and showed relative activities of 100:81:33:42 for euthermic PKC and 100:91:45:35 for hibernator PKC with phosphatidylserine, phosphatidylinositol, phosphatidylcholine, and phosphatidylethanolamine (each at 50 microM), respectively. Activation of bat PKC by phosphatidylserine was temperature sensitive, being 3.5-fold at 4 degrees C (hibernating body temperature) compared with 14-18-fold at 33 degrees C (near euthermic body temperature). Arrhenius plots for bat brain PKC showed a sharp break below 10 degrees C; activation energies below this temperature were 11.5- and 5.2-fold greater than at higher temperatures for the enzyme from hibernating versus euthermic animals. By contrast, plots for the rat enzyme were linear over the range 0-42 degrees C. The data suggest that a sharp suppression of PKC activity by several mechanisms (reduced total activity, low temperature effects on activity and sensitivity to phospholipids) may be important to overall metabolic rate suppression during hibernation.

Animals↗
PubMed1997

Metabolic regulation in mammalian hibernation: enzyme and protein adaptations.

Mammalian hibernation requires specific regulatory controls on metabolism to coordinate entry, maintenance, and arousal stages, as well as adjustments to many metabolic functions to support long-term dormancy. Several mechanisms of metabolic regulation are involved in potentiating survival. One of these is the reversible phosphorylation of regulatory enzymes, including glycogen phosphorylase, phosphofructokinase, pyruvate kinase, and pyruvate dehydrogenase. In particular, the sharp suppression of pyruvate dehydrogenase during hibernation shows the importance of control over mitochondrial oxidative metabolism for reducing metabolic rate. Fine control over specific enzymes also occurs via differential temperature effects on kinetic and allosteric properties. Analysis of temperature effects on the properties of pyruvate kinase, fructose-1,6-bisphosphatase, creatine kinase, and citrate synthase from ground squirrel or bat tissues shows a range of responses, some that would reduce enzyme activity in the hibernating state and some that would promote temperature-insensitive enzyme function. Reduced tissue phosphagen and adenylate levels, but not energy charge, may also contribute to overall metabolic suppression. New research is exploring the role of transcriptional and translational controls in hibernation via several approaches. For example, immunoblotting with antibodies to heat shock proteins (hsp 70 family) revealed the presence of constitutive hsc 70 in bat tissues but levels of the protein did not change between euthermic and hibernating states and neither the inducible hsp 70 nor the glucose-responsive protein grp 78 appeared during hibernation.

Adaptation, Physiological↗
PubMed1996

Occurrence of a differential expression of the glyceraldehyde-3-phosphate dehydrogenase gene in muscle and liver from euthermic and induced hibernating jerboa (Jaculus orientalis).

A cDNA clone which contains the near-complete open reading frame (ORF) encoding glyceraldehyde-3-phosphate dehydrogenase (GAPDH, EC 1.2.1.12) was obtained by screening a muscle cDNA library of jerboa (Jaculus orientalis), a true hibernating rodent, with a PCR-amplified 0.5-kb genomic DNA probe from an internal region of the gene. The 1.1-kb cDNA clone consists of a 927-bp ORF which codifies for 309 aa, about 93% of the original GapC gene encoding the 36-kDa protein, and a 3'-noncoding region of 167 bp. The full-length aa sequence of GAPDH was achieved by sequencing the N-terminal region of the purified protein completing the missing part in the cDNA clone. Both nt and aa sequences exhibit a high degree of homology to other mammalian GAPDHs. The expression of the GapC gene was studied in skeletal muscle and liver of euthermic and hibernating jerboas both on the mRNA level by Northern blot hybridization using the cDNA clone as a probe and on the protein level by Western blot immunodetection using an antibody raised against muscle GAPDH. A clear decrease (about threefold) in the amount of GapC mRNA, a single 1.2-kb transcript, was observed in muscle of hibernating jerboa when compared with the same tissue from the euthermic animal. This mRNA level decrease directly correlates with a reduction in both protein amount and specific activity in crude protein extracts. In contrast, both GAPDH protein and GapC mRNA levels remained unchanged in liver from euthermic and hibernating jerboas although the enzymatic activity was also about threefold lower in the hibernating tissue. These result, together with previous data obtained from protein studies [Soukri et al. (1995) Biochim. Biophys. Acta 1243, 161-168 and (1996) 1292, 177-187] indicate that jerboa GAPDH is regulated by different mechanisms during hibernation in these tissues, that is, at transcriptional level in muscle and at posttranslational level in liver. The reduced GAPDH activity should result in both cases in a decrease of the glycolytic flux that would eventually contribute to the dramatic metabolic depression of this dormant state.

Amino Acid Sequence↗
PubMed1998

Immunocytochemical changes of cytoskeleton components and calmodulin in the frog cerebellum and optic tectum during hibernation.

During hibernation, variation in the metabolism of nerve cells occurs. Since the cytoskeleton plays an important role in nerve cell function, we have analyzed the immunocytochemical expression of two cytoskeleton components, i.e. phosphorylated 200 kDa neurofilament protein, and microtubule-associated protein 2 in the cerebellum and optic tectum of hibernating frogs (Rana esculenta) in comparison with active animals. In addition, we have considered the immunocytochemical expression of calmodulin, which is known to be involved in neurofilament phosphorylation. In hibernating animals, there was a decrease in the immunoreactivity for phosphorylated 200 kDa neurofilament protein and microtubule-associated protein 2 of fibers in both the cerebellum and in the optic tectum. In contrast, in the large neurons of the cerebellum, i.e. Purkinje neurons, there was an increase in the immunoreactivity for microtubule-associated protein 2. The changes in the cytoskeleton components were accompanied by a decrease in calmodulin immunoreactivity in the cytoplasm of nerve cells of the cerebellum. All the changes observed are consistent with a low neuronal activity during hibernation, as also indicated by previous microdensitometric and microfluorometric data. This shows a higher degree of chromatin condensation in hibernating animals and suggests that hibernation represents a simple form of neuronal plasticity.

Animals↗
PubMed2003

Hibernation reduces pancreatic amylase levels in ground squirrels.

Pancreatic enzyme levels in mammals are influenced by food intake and dietary composition. In this study, we examined the activity and expression of pancreatic amylase in a hibernating mammal, a natural model for long-term fasting. Pancreatic tissues were obtained from summer-active 13-lined ground squirrels and hibernating squirrels that had not eaten for at least 6 weeks. Amylase specific activity was reduced by approximately 50% in the torpid hibernators compared with summer squirrels, and immunoblot analysis revealed that amylase protein expression was reduced by approximately 40% in the hibernators. Similar reductions in amylase specific activity were observed in interbout euthermic hibernators. These results support a strong influence of food intake on pancreatic enzyme expression in hibernating mammals. The maintenance of basal levels of this key digestive enzyme at approximately 50% of summer values despite the extended winter fast likely facilitates the rapid resumption of digestive function after terminal arousal in the spring.

Amylases↗
PubMed2003

Control of breathing in the echidna (Tachyglossus aculeatus) during hibernation.

Resting non-hibernating echidnas are characterised by low metabolic rates, but also have a very low respiratory frequency and a variable respiratory minute volume, often resulting in low levels of arterial O(2) and high CO(2). As the echidna lies at one physiological extreme among the hibernators, in terms of its large size and low metabolism and ventilatory requirement when not hibernating, a study of control of breathing during hibernation in echidnas should provide a useful test of the generality of various models. We used non-invasive techniques to study breathing patterns and the control of ventilation in 6 echidnas. Hibernating echidnas (T(b) range 7-10 degrees C) showed episodic breathing with bursts of breaths (average 36+/-16 breaths in 24+/-5 min) followed by a period of apnea (76+/-17 min) then a series (8+/-4) of slow breaths at 14+/-1 min intervals leading up to the next burst. Increasing CO(2) levels in the inspired air increased the number of breaths in a burst, eventually leading to continuous breathing. Inter burst breaths were controlled by O(2): hypoxia increased inter burst breaths, and decreased burst length, while hyperoxia abolished inter burst breaths and increased the apneic period. Overall, while CO(2) was a strong respiratory stimulus in hibernating echidnas, O(2) had little effect on total ventilation, but did have a strong effect on the breathing pattern.

Animals↗
PubMed2000

Age affects hibernation in Syrian hamsters (Mesocricetus auratus).

In this study, we aimed to show how age affects hibernation in the Syrian hamster. Experimentally, we used 30 male animals differing in age. The old animals were 20 months of age and the adults were 8 months of age at the end of the test. The young animals were 3 weeks old at the start of testing and 5 months old at the end of the testing period. The torpor observation started October 15, 1996, and ended March 11, 1997, in the laboratory colony maintained under natural photoperiod and outdoor air. Observations were performed around noon daily. Three measures (i.e., prehibernation period [hibernation latency], proportion of hibernation spent in torpor, and proportion of animals in torpor), all of which reflect the strength of occurrence of hibernation, indicated that the older hamsters (1) started hibernation earlier, (2) spent more time in torpor, and (3) had a higher chance of being in torpor than the younger ones during the hibernation season.

Aging↗
PubMedDate not supplied

Myosin isoform expression and MAFbx mRNA levels in hibernating golden-mantled ground squirrels (Spermophilus lateralis).

Hibernating mammals present many unexplored opportunities for the study of muscle biology. The hindlimb muscles of a small rodent hibernator (Spermophilus lateralis) atrophy slightly during months of torpor, representing a reduction in the disuse atrophy commonly seen in other mammalian models. How torpor affects contractile protein expression is unclear; therefore, we examined the myosin heavy-chain (MHC) isoform profile of ground squirrel skeletal muscle before and after hibernation. Immunoblotting was performed first to identify the MHC isoforms expressed in this species. Relative percentages of MHC isoforms in individual muscles were then measured using SDS-PAGE (sodium dodecyl sulfate-polyacrylamide gel electrophoresis). The soleus and diaphragm did not display differences in isoforms following hibernation, but we found minor fast-to-slow isoform shifts in MHC protein in the gastrocnemius and plantaris. These subtle changes are contrary to those predicted by other models of inactivity but may reflect the requirement for shivering thermogenesis during arousals from torpor. We also measured mRNA expression of the Muscle Atrophy F-box (MAFbx), a ubiquitin ligase important in proteasome-mediated proteolysis. Expression was elevated in the hibernating gastrocnemius and the plantaris but was not associated with atrophy. Skeletal muscle from hibernators displays unusual plasticity, which may be a combined result of the intense activity during arousals and the reduction of metabolism during torpor.

Animals↗
PubMedDate not supplied

Protein use and muscle-fiber changes in free-ranging, hibernating black bears.

Studies of the metabolic and physiological changes that bears undergo during hibernation have, for the most part, supported the paradigm that bears use only fatty tissues as a metabolic substrate during hibernation. This study was performed to document the extent of protein loss and alteration of muscle-fiber characteristics of selected muscles in black bears during winter dormancy. Muscle biopsies were removed from the gastrocnemius and biceps femoris from seven free-ranging female black bears on the Uncompahgre Plateau in west-central Colorado. Six of the seven bears produced cubs during the hibernating season. Muscle samples were collected from the left hind limb shortly after bears entered their dens (fall), and additional samples were collected from the right hind limb just prior to bears leaving their dens (spring). Protein concentration, fast- and slow-twitch muscle-fiber ratios and muscle-fiber cross-sectional areas, and citrate synthase activity were measured in the laboratory. While protein concentration decreased in both muscles during the hibernation period, it was lower than predicted for lactating females. In addition, muscle-fiber number and cross-sectional area were unchanged in these muscles, suggesting only limited muscle atrophy. In support of these observations, there was a moderate but significant increase in the proportion of fast-twitch fibers only in the biceps femoris, with a concomitant decrease in citrate synthase activity, but no alteration of the fiber ratio in the gastrocnemius during hibernation. These findings suggest that hibernating bears, particularly lactating females, do use some protein, in concert with fat catabolism, as a metabolic substrate and as a source of water. However, the extent of this protein use is moderate and is associated with limited alteration of muscle structure, characteristic of disuse atrophy.

Animals↗
PubMed1985

Ventricular repolarization and fibrillation threshold in hibernating species.

Hibernators are resistant to ventricular fibrillation (VF) induced by hypothermia. This is in contrast to non-hibernating mammals which develop circulatory arrest, usually VF, in the temperature region 15-20 degrees C. The hedgehog which is a hibernator showed resistance to VF also when VF-evoking procedures other than hypothermia were used, such as local application of aconitine on the epicardium, administration of 0.55 M CaCl2 to isolated hearts perfused with a potassium-free modified Tyrode solution, injection of procaine HCl into isolated hearts perfused with a modified Tyrode solution after previous adrenaline administration, and ligation of the left descending coronary artery. Electrical stimulation in the vulnerable period produced VF in some but not in all the hedgehogs but a greater current was necessary than in guinea-pigs, all of which developed VF. Factors of possible importance to explain this difference in VF resistance are the QT duration which is short in hibernators, adrenergic innervation (ventricular muscle fibres in hibernators lack sympathetic innervation), metabolic factors (different temperature activity curves in hibernators compared to nonhibernating mammals) and ultrastructure (less skeletin filament in the conduction system of the hedgehog heart).

Aconitine↗
PubMed1999

Ultrastructure of taste receptor cells in active and hibernating ground squirrels.

Differences in taste bud ultrastructure between active and low-temperature hibernation states were investigated in the Siberian ground squirrel, Citellus undulatus. Compared to active summer animals, taste bud volume and the morphology of the taste pore showed little change while an animal was hibernating. However, impressive differences were observed in nuclei and cytoplasmic organelles of all cells within taste buds. In low-temperature hibernation the nucleoli of elongated, non-dark cells had few, but large, fibrillar centres, a sign of inactivity. In the cytoplasm, the number of free polyribosomes (polysomes) was sharply decreased; ribosomes were seen mainly as (non-synthesizing) monosomes and more seldom as membrane-associated ribosomes. Profiles of endoplasmic reticulum (ER) were reduced, to the extent that only separate and rare cisternae of smooth and rough ER remained. The large vacuoles, which are typically found in many taste cells of active animals, were absent during hibernation, and the Golgi apparatus appeared to be disassembled into numerous vesicles. Of these, many had small diameters near 60 nm, while a few had larger diameters near 300 nm. Secretory organelles (dense granules in dark cells and dense-cored vesicles in type III cells) were rare during hibernation, the lateral plasma membrane was smooth, and signs of exocytosis were not found. These changes suggest reduced protein synthesis and reduced sensory function during hibernation.

Animals↗
PubMed1998

Hibernation in ground squirrels induces state and species-specific tolerance to hypoxia and aglycemia: an in vitro study in hippocampal slices.

Hibernation in mammals is associated with a regulated depression of global cellular functions accompanied by reductions of cerebral blood flow that would render the brain profoundly ischemic under normal conditions. Homeostatic control is preserved, however, and brain damage does not occur. We investigated the possibility that hibernation not only confers tolerance to profound hypothermia, but also to hypoxia and aglycemia independent of temperature. Hippocampal slices from ground squirrels Citellus tridecemlineatus in both the active and hibernating states and from rats were subjected to in vitro hypoxia and aglycemia at incubation temperatures of 36 degrees C, 20 degrees C, and 7 degrees C and evaluated histologically. A binary bioassay was used to determine the duration of hypoxia/aglycemia tolerated in each group. At all temperatures, slices from hibernating animals were most tolerant compared with both active squirrels and rats. Slices from active ground squirrels were more tolerant than rat at 20 degrees C and 7 degrees C but not at 36 degrees C indicating a species-specific difference that becomes manifest at lower temperatures. These results indicate that hibernation is associated not only with tolerance to profound hypothermia but also to deprivation of oxygen and glucose. Because tolerance was already demonstrable at the shortest duration of hibernation studied, rapid therapeutic induction of a similar state may be possible. Therefore, identification of the regulatory mechanisms underlying this tolerance may lead to novel neuroprotective strategies.

Adaptation, Physiological↗
PubMed2002

Reversible impairment of endothelium-dependent relaxation in golden hamster carotid arteries during hibernation.

The effects of hibernation on endothelium-dependent vasodilatation were investigated in the golden hamster carotid artery, paying special attention to hibernating body temperature (10 degrees C). To record mechanical and electrical membrane responses, we applied pharmacological (organ bath) and electrophysiological (microelectrode) techniques, using acetylcholine (ACh; 0.001-100 microM) and ATP (0.01-1000 microM) for endothelium-dependent vasodilatation and sodium nitroprusside (SNP; 0.05-10 microM) for endothelium-independent vasodilatation. At 34 degrees C, ACh, ATP and SNP each induced a relaxation or a hyperpolarization, and these responses were similar in all the preparations from control and hibernated animals. At 10 degrees C, on the other hand, ACh-induced relaxations and hyperpolarizations were reduced to approximately 35 % and 50 % of the euthermic level in controls and 1 % and 4 % of the euthermic level in hibernated animals, respectively. In contrast, at 10 degrees C, ATP induced only a contraction or depolarization in all preparations with no significant difference between control and hibernated animals. SNP-induced relaxations and hyperpolarizations obtained at 34 degrees C were not attenuated by cooling to 10 degrees C. In the presence of a P2X receptor blocker, pyridoxal phosphate-6-azophenyl-2',4'-disulphonic acid (PPADS; 5 microM), at 34 degrees C ATP-induced relaxations and hyperpolarizations were significantly enhanced whereas no responses were induced by ATP at 10 degrees C. After endothelium removal, on the other hand, ATP induced only a contraction or depolarization at both 34 degrees C and 10 degrees C. These results suggest that depression of endothelium-dependent vasodilator responses to ACh and ATP may occur in the hibernating golden hamster carotid artery.

Acetylcholine↗
PubMed1976

Changes in CNS responsiveness during hibernation.

The ability of the midbrain reticular formation (MRF) to produce thermogenic responses and to trigger arousal from hibernation was tested during successive quarters of individual hibernation bouts. Golden-mantled ground squirrels (Citellus lateralis) were implanted with bilateral cannula guides into the MRF. Single, bilateral, 1-mul injections of acetylcholine (ACh) at concentrations of 50, 100, or 200 mug/mul were delivered in each quarter of the same bout or in selected quarters of different bouts. The results show that the magnitude of thermogenic responses evoked by ACh stimulation of the MRF was depressed during the early portion of the bout and increased as time in the bout elapsed. Furthermore, the magnitude of responses evoked during hibernation was depressed in comparison to those evoked during euthermia, indicating the influence of inhibition on the responsiveness of the CNS during hibernation. We suggest that during hibernation, a progressive change in responsiveness of the CNS, perhpas focused in the MRF, controls the duration of each hibernation bout.

Acetylcholine↗
PubMed2003

Inhibition of hibernation by exercise is not affected by intergeniculate leaflets lesion in hamsters.

The circadian clock of mammals, located in the suprachiasmatic nuclei (SCN) of the hypothalamus, has been demonstrated to integrate day length change from long (LP) to short photoperiod (SP). This photoperiodic change induces in Syrian hamsters a testicular regression through melatonin action, a phenomenon that is inhibited when hamsters have free access to a wheel. The intergeniculate leaflets (IGL), which modulate the integration of photoperiod by the SCN, are a key structure in the circadian system, conveying nonphotic information such as those induced by novelty-induced wheel running activity. We tested in hamsters transferred from LP to a cold SP the effects of wheel running activity on a photoperiod-dependent behavior, hibernation. Lesions of the IGL were done to test the role of this structure in the inhibition induced by exercise of photoperiod integration by the clock. We show that wheel running activity actually inhibits hibernation not only in sham-operated animals, but also in hamsters with a bilateral IGL lesion (IGLX). In contrast, IGL-X hamsters without a wheel integrate slower to the SP but hibernate earlier compared with sham-operated animals. Moreover, some hibernation characteristics are affected by IGL lesion. Throughout the experiment at 7 degrees C, IGL-X hamsters were in hypothermia during 18% of the experiment vs. 32% for sham-operated hamsters. Taken together, these data show that the IGL play a modulatory role in the integration of photoperiodic cues and modulate hibernation, but they are not implicated in the inhibition of hibernation induced by wheel running activity.

Animals↗
PubMed1977

CNS regulation of body temperature in euthermic and hibernating marmots (Marmota flaviventris).

Hypothalamic thermosensitivity of marmots was characterized during euthermia and hibernation. Hypothalamic temperature (Thy) was manipulated with chronically implanted, water-perfused thermodes while the animal's rate of oxygen consumption was continuously measured. The threshold Thy for eliciting an increase in metabolic heat production (MHP) and the proportionality constant (alphaMHP) relating rate of MHP to Thy were determined. In four euthermic marmots alphaMHP averaged -1.1 W-kg-1-degrees C-1. During the entrance into hibernation, as body temperature (Tb) declined from 36 to 8 degrees C, the threshold Thy for the MHP response progressively declined and was demonstrable at all times. The Thy of marmots in deep hibernation at an ambient temperature (Ta) of 5 degrees C plateaued near 7.5 degrees C, but threshold Thy for MHP showed a continuous slow decline of 0.2-0.4 degrees C a day, until one day prior to arousal. Proportional regulation of Tb was demonstrable at all times during deep hibernation. The average proportionality constant for the MHP response to hypothalamic cooling during deep hibernation in three marmots was -0.08 W-kg-1-degrees C-1. These results demonstrate that the hypothalamic regulator of Tb is active throughout hibernation and that there are progressive changes in its thermosensitivity.

Animals↗
PubMed1989

Brown fat GDP binding and circulating metabolites during hibernation and arousal.

The effect of hibernation and arousal on brown adipose tissue (BAT) cytochrome-c oxidase activity and GDP binding, as well-circulating metabolites, have been studied in the 13-lined ground squirrel. Control animals (warm adapted) were housed continuously at 23 degrees C, while the remaining animals were transferred into a cold room (4 degrees C) for 8 days to induce hibernation. Hibernating animals were killed while deeply hibernating. Aroused animals were manually stimulated to induce arousal or had spontaneously aroused on the day of the experiment. BAT weight as well as mitochondrial mass were increased in both groups of cold-adapted animals, relative to controls. A substantial increase in GDP binding, however, was seen only in aroused animals, an observation confirmed by Scatchard analysis. Arousal was also accompanied by marked alterations in the levels of several circulating metabolites. Plasma free fatty acids declined by approximately 20% despite a three- to fourfold increase in plasma glycerol concentrations. Plasma lactate levels increased eightfold, while concentrations of beta-hydroxybutyrate were five times lower during arousal than hibernation. These data are consistent with the idea that the oxidation of free fatty acids, glucose, and ketone bodies are all increased during arousal. In conclusion, we have found that cold adaptation and subsequent hibernation increases BAT thermogenic capacity in the 13-lined ground squirrel. However, this increase in thermogenic potential is not manifested as a substantial increase in BAT thermogenic activity until arousal is initiated.

Adipose Tissue, Brown↗
PubMed1991

Are ground squirrels sleep deprived during hibernation?

Hibernation is an adaptation for energy conservation, which probably evolved as an extension of non-rapid-eye-movement sleep mechanisms. Yet, during periodic arousals from bouts of deep hibernation, ground squirrels (Spermophilus lateralis) spend most of their time asleep. Spectral analysis of the electroencephalogram revealed that cortical slow-wave intensity during sleep is high at the beginning of a euthermic period and declines thereafter. Sleep slow-wave intensity is greater after longer bouts of hibernation than after shorter bouts. We hypothesize that low body temperatures during hibernation are incompatible with the restorative function of sleep as reflected in cortical slow-wave activity. Animals must incur the energetic costs of periodic arousals from hibernation to receive the restorative benefits of euthermic slow-wave sleep. The timing of arousals from hibernation may be a function of accumulated sleep debt.

Animals↗