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PubMed1995

The cerebral neurons of Helix aspersa during hibernation. Changes in the cytochemical detection of calmodulin, cytoskeletal components and phosphatases.

Some markers of the intracellular systems that regulate neuronal activity and morphology were analyzed in the cerebral ganglion of hibernating snails (Helix aspersa), in comparison with active animals. The immunocytochemical expression of a calcium-binding protein, i.e. calmodulin, and some cytoskeletal components, i.e. 200 kDa phosphorylated neurofilament protein (pNFH), microtubule associated protein 2 (MAP2) and alpha-tubulin were analyzed by the use of a panel of antibodies raised against mammal antigens. Moreover, by enzymatic reactions the Ca(2+)-ATPase and alkaline phosphatase (AIPase) activities were demonstrated. In comparison with the active phase, the hibernation induced an increase in the immunopositivity for calmodulin in all the neurons. The increase may be linked to unmasking of immunoreactive epitopes due to conformational changes of the protein, which in turn may be a consequence of a reduction or absence of binding with calcium ions or of a real increase in the amount of calmodulin in the somata of neurons. In any event, both the hypotheses indicate that neurons have decreased or suppressed the Ca(2+)-dependent mechanisms as also shown by the lower Ca(2+)-ATPase activity. Nevertheless, the AIPase activity, which was localized in the epineural sheat, was not significantly changed during hibernation and this supports that some metabolic activities are preserved in the hibernated animals. Changes in the immunopositivity for cytoskeletal components were found. There was an increase in the epitopes recognized by the mammalian pNF antibody, that concerned both the positivity of the entire cytoplasm of some clusters of metacerebral neurons and the intensity of the reaction. This would be aimed to improve the stability of the somata and primary neurites. Moreover, the decrease of alpha-tubulin and MAP2 immunopositivity, suggests that a disassembly of microtubules have occurred. The findings indicate that the transport of vesicles in the axons is slowed down during hibernation. In fact, research in progress show that the patterns of neurotransmission and neuromodulation are also deeply modified.

Alkaline Phosphatase↗

PubMed2001

Differential expression of adipose- and heart-type fatty acid binding proteins in hibernating ground squirrels.

The up-regulation of heart- and adipose-type fatty acid binding proteins (H-FABPs and A-FABPs) was detected during hibernation in brown adipose tissue (BAT) of 13-lined ground squirrels, Spermophilus tridecemlineatus, using a commercial rat cDNA array. Full length cDNAs encoding H-FABPs and A-FABPs were subsequently retrieved from a BAT cDNA library. These cDNAs were used to probe Northern blots of total RNA from tissues of euthermic versus hibernating ground squirrels. H-FABP mRNA transcripts increased in BAT, skeletal muscle and heart of hibernating animals whereas A-FABP transcripts, which are normally expressed exclusively in adipose tissue, increased in both BAT and heart during torpor. It is proposed that the increased expression of H-FABPs and A-FABPs during hibernation accelerates the rate at which fatty acids can be transported to the mitochondria for oxidization, particularly in support of the huge increase in thermogenesis by BAT and rapid increase in heart rate that are required during arousal from torpor. Comparison of the deduced polypeptide sequence of ground squirrel H-FABP with that from other mammals also revealed three unique amino acid differences which may be important for protein function at low body temperatures during hibernation.

Adipose Tissue↗

PubMed1999

Reduced epinephrine-stimulated lipolytic activity in male golden-mantled ground squirrel during hibernation: an in situ microdialysis study.

We studied lipolytic activities in vivo in golden mantle ground squirrels during pre-hibernation and hibernation using microdialysis technique. Microdialysis probes were inserted into the abdominal subcutaneous adipose tissues. Baseline lipolysis were assessed by measuring glycerol concentration. Epinephrine-stimulated lipolysis was also examined. Eight squirrels (four male, four female) were studied in each of the two stages. Basal glycerol concentrations were lower in the hibernating state than in the pre-hibernation state in male squirrels (P < 0.05). Epinephrine application induced glycerol release in male and female squirrels (P < 0.001) in both stages. Male squirrels demonstrated a reduced epinephrine-stimulated glycerol release in the hibernating state, which was not observed in female squirrels.

Adipose Tissue↗

PubMed1997

Expression of multiple alpha1-antitrypsin-like genes in hibernating species of the squirrel family.

In the chipmunk, a mammalian hibernator, a 140 kDa protein complex found in the blood, drastically decreases in concentration during hibernation. This complex contains four species of proteins, HP-20, -25, -27 and -55. In the present study, cDNA clones coding for the chipmunk HP-55 were isolated from a liver cDNA library. Sequence analysis revealed that HP-55 is produced as a precursor protein of 413 amino acids (aa), that it has a signal peptide of 24 aa, and that it contains four potential N-glycosylation sites. The deduced aa sequence shows 63% identity with that of rat alpha1-antitrypsin (alpha1-AT); however, the sequence corresponding to the reactive center P1-P1' residues was found to be Met-Leu, whereas it is Met-Ser in the rat alpha1-AT. During screening of the chipmunk liver cDNA library, four other related classes of cDNA clones were obtained, each also coding for an alpha1-AT-like protein. In spite of more than 86% overall aa sequence identity among the five chipmunk alpha1-AT-like proteins, they are highly divergent in the putative reactive center region; the putative P1-P1' sequences are Met-Leu (HP-55 or CM55-ML), Met-Met (CM55-MM), Met-Ser (CM55-MS), Ser-Ile (CM55-SI) and Ser-Thr (CM55-ST). Each of the alpha1-AT-like protein mRNAs was expressed in chipmunk liver, and the HP-55 mRNA level was greatly reduced during hibernation. Genomic Southern blot analysis and screening of a liver cDNA library from another hibernating squirrel species, the ground squirrel, also revealed expression of multiple members of the alpha1-AT gene family, whereas analysis of a cDNA library from a non-hibernating species, the tree squirrel, found only a single alpha1-AT gene.

Amino Acid Sequence↗

PubMed1997

Neurochemical coding in the myenteric plexus of the upper gastrointestinal tract of hibernating hamsters.

As part of our investigation of the plasticity of autonomic nerves in physiological and pathological conditions, we have examined the effect of hibernation on the neurochemical content of myenteric nerves and nerve cell bodies of the upper gastrointestinal tract of the non-seasonal hibernator, the golden hamster. Age matched hamsters kept at room temperature and those kept at 5 degrees C but which failed to hibernate, were used as controls. Possible changes in nerve fibres and nerve cell bodies containing the general neuronal marker, protein gene product 9.5, the peptides, vasoactive intestinal polypeptide, substance P (SP) and calcitonin gene-related peptide (CGRP), the catecholamine synthesizing enzyme tyrosine hydroxylase and the enzyme responsible for synthesizing nitric oxide, nitric oxide synthase, were examined in the oesophagus, proventriculus and proximal and distal stomach of the golden hamsters using immunohistochemical techniques. The results of the present study revealed a significant increase in the number of nerve cell bodies and density of nerve fibres containing SP-immunoreactivity and increased number of CGRP-immunoreactive cell bodies but not the other markers examined in the proximal stomach and proventriculus. In contrast, there was no change in the distribution of any of the neuroactive substances examined in the myenteric plexus of the oesophagus and distal stomach. It is suggested that the change in the environment of the hibernating hamsters perturbs the normal digestive physiology in the proximal stomach and proventriculus that is reflected by the selective changes in SP- and CGRP-containing enteric nerves; these changes may be part of protective reflex mechanisms to the environmental changes resulting from hibernation, where upgrading of nerve cell bodies expressing CGRP and SP has occurred.

Animals↗

PubMed1998

Uncoupling protein mRNA, mitochondrial GTP-binding, and T4 5'-deiodinase activity of brown adipose tissue in Daurian ground squirrel during hibernation and arousal.

The mRNA level of uncoupling protein (UCP) specific for brown adipose tissue (BAT) in Daurian ground squirrel, was detected by using a [32P]-labeled oligonucleotide probe. The UCP concentration in mitochondria was indirectly determined by titration with its specific ligand [H3]-labeled GTP. Type II T4 5'-deiodinase of BAT was assayed concomitantly. We found two species of mRNA for UCP with lengths of about 1.9 and 1.5 kb, respectively, both occurring in almost the same concentration. UCP mRNA content was elevated significantly during hibernation, but the UCP concentration did not change compared with that of nonhibernating controls kept at room temperature. When hibernating squirrels were aroused, the UCP mRNA remained at the elevated level as during hibernation, but the UCP concentration increased in comparison with that of nonhibernating controls or during hibernating. Changes in T4 5'-deiodinase activity in BAT were similar to the variations of the UCP mRNA level. These results suggest that the activation of T4 5'-deiodinase in BAT may be an important factor for the up-regulation and maintenance of UCP mRNA content needed for the synthesis of sufficient UCP to acquire the thermogenic capacity for arousal from hibernation.

Adipose Tissue↗

PubMed1988

Calorimetric and spectroscopic studies of lipid thermotropic phase behavior in liver inner mitochondrial membranes from a mammalian hibernator.

Arrhenius plots of various enzyme and transport systems associated with the liver mitochondrial inner membranes of ground squirrels exhibit changes in slope at temperatures of 20-25 degrees C in nonhibernating but not in hibernating animals. It has been proposed that the Arrhenius breaks observed in nonhibernating animals are the result of a gel to liquid-crystalline phase transition of the mitochondrial membrane lipids, which also occurs at 20-25 degrees C, and that the absence of such breaks in hibernating animals is due to a major depression of this lipid phase transition to temperatures below 4 degrees C. In order to test this hypothesis, we have examined the thermotropic phase behavior of liver inner mitochondrial membranes from hibernating and nonhibernating Richardson's ground squirrels, Spermophilus richardsonii, by differential scanning calorimetry and by 19F nuclear magnetic resonance and fluorescence polarization spectroscopy. Each of these techniques indicates that no lipid phase transition occurs in the membranes of either hibernating or nonhibernating ground squirrels within the physiological temperature range of this animal (4-37 degrees C). Moreover, differential scanning calorimetric measurements indicate that only a small depression of the lipid gel to liquid-crystalline phase transition, which is centered at about -5 degrees C in nonhibernating animals and at about -9 degrees C in hibernators, occurs. We thus conclude that the Arrhenius plot breaks observed in some membrane-associated enzymatic and transport activities of nonhibernating animals are not the result of a lipid phase transition and that a major shift in the gel to liquid-crystalline lipid phase transition temperature is not responsible for seasonal changes in the thermal behavior of these inner mitochondrial membrane proteins.

Acclimatization↗

PubMed2003

Neuropeptide modulation of evoked responses of neurons in the medial septal region of hibernating ground squirrels in conditions of chronic isolation of the medial septal region from preoptic-hypothalamic structures.

Septal slices from hibernating ground squirrels were initially (for two weeks) subjected to basal separation of the septal region and were then used for studies of the effects of neuropeptides extracted from the brains of hibernating animals (TSKYR, TSKY, and DY) and monoaminergic neurotransmitters (noradrenaline and serotonin) on neuronal responses evoked by intraseptal electrical stimulation. Despite removal of a large complex of afferent connections and direct contacts with the preoptic region, the neurons retained their normal reactivity and the normal distribution of response types. Neuropeptides efficiently modulated responses, and had strong facilitatory effects on oligosynaptic short-latency responses consisting of single spikes. In most cases (78% of tests), effects on evoked activity were independent of effects on baseline discharge frequency. These data lead to the suggestion that neuropeptides have two influences on septal neurons: a direct, non-synaptic influence on the pacemaker potential responsible for baseline activity, and modulation of synaptic processes. Analysis showed that retention of descending septohippocampal connections was not critical for entry into hibernation and the tonic maintenance of this state. The effects of preoptic-hypothalamic mechanisms of hibernation determine the paradoxical latent excitability of septal cells, allowing the septohippocampal system to filter external signals and provide for urgent arousal of the forebrain during hibernation.

Animals↗

PubMed2002

Climate-mediated energetic constraints on the distribution of hibernating mammals.

To predict the consequences of human-induced global climate change, we need to understand how climate is linked to biogeography. Energetic constraints are commonly invoked to explain animal distributions, and physiological parameters are known to vary along distributional gradients. But the causal nature of the links between climate and animal biogeography remain largely obscure. Here we develop a bioenergetic model that predicts the feasibility of mammalian hibernation under different climatic conditions. As an example, we use the well-quantified hibernation energetics of the little brown bat (Myotis lucifugus) to parameterize the model. Our model predicts pronounced effects of ambient temperature on total winter energy requirements, and a relatively narrow combination of hibernaculum temperatures and winter lengths permitting successful hibernation. Microhabitat and northern distribution limits of M. lucifugus are consistent with model predictions, suggesting that the thermal dependence of hibernation energetics constrains the biogeography of this species. Integrating projections of climate change into our model predicts a pronounced northward range expansion of hibernating bats within the next 80 years. Bioenergetics can provide the simple link between climate and biogeography needed to predict the consequences of climate change.

Animal Migration↗

PubMed1978

Changes in the form of Arrhenius plots of the activity of glucagon-stimulated adenylate cyclase and other hamster liver plasma-membrane enzymes occurring on hibernation.

1. Arrhenius plots of the glucagon-stimulated adenylate cyclase, 5'-nucleotidase, (Na+ + K+)-stimulated adenosine triphosphatase and Mg2+-dependent adenosine triphosphatase activities of control hamster liver plasma membranes exhibited two break points at around 25 and 13 degrees C, whereas Arrhenius plots of their activities in hibernating hamster liver plasma membranes exhibited two break points at around 25 and 4 degrees C. 2. A single break occurring between 25 and 26 degrees C was observed in Arrhenius plots of the activities of fluoride-stimulated adenylate cyclase, basal adenylate cyclase and cyclic AMP phosphodiesterase of liver plasma membranes from both control and hibernating animals. 3. Arrhenius plots of phosphodiesterase I activity showed a single break at 13 degrees C for membranes from control animals, and a single break at around 4 degrees C for liver plasma membranes from hibernating animals. 4. The temperature at which break points occurred in Arrhenius plots of glucagon- and fluoride-stimulated adenylate cyclase activity were decreased by about 7--8 degrees C by addition of 40 mm-benzyl alcohol to the assays. 5. Discontinuities in the Arrhenius plots of 4-anilinonaphthalene-1-sulphonic acid fluorescence occurred at around 24 and 13 degrees C for liver plasma membranes from control animals, and at around 25 and 4 degrees C for membranes from hibernating animals. 6. We suggest that in hamster liver plasma membranes from control animals a lipid phase separation occurs at around 25 degrees C in the inner half of the bilayer and at around 13 degrees C in the outer half of the bilayer. On hibernation a change in bilayer asymmetry occurs, which is expressed by a decrease in the temperature at which the lipid phase separation occurs in the outer half of the bilayer to around 4 degrees C. The assumption made is that enzymes expressing both lipid phase separations penetrate both halves of the bilayer, whereas those experiencing a single break penetrate one half of the bilayer only.

Adenylyl Cyclases↗

PubMed2004

Genes controlling the metabolic switch in hibernating mammals.

Hibernating mammals have the ability to decrease their metabolic rate and survive up to 6 months without food in an inactive state where body temperatures approach 0 degrees C. In hibernating 13-lined ground squirrels (Spermophilus tridecemlineatus), oxygen consumption holds at 1/30 to 1/50 of the aroused condition and heart rates are as low as 3-10 beats/min, compared with 200-300 beats/min when the animal is active. This seasonal adaptation requires a metabolic shift away from the oxidation of carbohydrates and towards the combustion of stored fatty acids as the primary source of energy. A key element in this fuel switch is the differential expression of the gene encoding pyruvate dehydrogenase kinase isoenzyme 4. Pyruvate dehydrogenase kinase isoenzyme 4 inhibits pyruvate dehydrogenase and thus minimizes carbohydrate oxidation by preventing the flow of glycolytic products into the tricarboxylic acid cycle. Hibernators also exploit the low-temperature activity of PTL (pancreatic triacylglycerol lipase) in both heart and white adipose tissue. Lipolytic activity at body temperatures associated with hibernation was examined using recombinant ground squirrel and human PTL expressed in yeast. Enzymes from both humans and ground squirrel displayed high activity at temperatures as low as 0 degrees C and showed Q(10) = 1.2-1.5 over the temperature range 37-7 degrees C. These studies indicate that low-temperature lipolysis is a general property of PTL and does not require protein modifications unique to mammalian cells and/or the hibernating state.

Animals↗

PubMed2006

Rapid and reversible changes in intrahippocampal connectivity during the course of hibernation in European hamsters.

The hippocampal formation is a highly plastic brain structure that undergoes structural remodeling in response to internal and external challenges such as metabolic imbalance and repeated stress. We investigated whether the extreme alterations in metabolic status that occur during the course of hibernation in European hamsters cause structural changes in the dendritic arborizations of the CA3 pyramidal neurons and their main excitatory afferents, the mossy fiber terminals (MFT), that originate in the dentate gyrus. We report that apical, but not basal, dendritic trees of Golgi-impregnated CA3 principal neurons are significantly shorter, less branched, and less spiny in hypothermic hamsters compared with active animals. After the induction of arousal from torpor, within 2 h, the apical dendritic lengths, branching patterns, and spine density estimations returned to levels found in active, euthermic hamsters. The ultrastructure of MFT in hibernating hamsters showed a significant reduction in synaptic vesicle density and in the percentage of MFT area covered by spine profiles. Awakened hamsters showed restoration of MFT morphology to that seen in active animals. MFT of torpid animals also showed a significant increase in the percentage area of mitochondrial profiles that remained higher 3 h after induced arousal from hibernation compared with euthermic controls. Thus, the torpid/awakening cycle of the hibernating European hamster causes a rapid and reversible morphological reorganization of intrahippocampal subregions involved in information processing. The reported reductions in morphological connectivity between the dentate gyrus and the CA3 subregions could underlie the cessation of exploratory activity and spatial navigation skills during hibernation.

Animals↗

PubMed1992

Central role for differential gene expression in mammalian hibernation.

Mammalian hibernators experience dramatic reductions in body temperature, metabolic rate, respiratory rate, and heart rate during hibernation. These changes are precisely controlled and reversible with only internally driven mechanisms, suggesting specific biochemical regulation. We present a model that integrates our observations of differential liver gene expression during preparation for, and maintenance of, the hibernating state, with the known phylogenetic interspersion of hibernating species in several major mammalian lineages. This model predicts a major role for the differential expression of existing mammalian genes in the biochemical regulation of hibernation.

Animals↗

PubMed1996

Ablation of suprachiasmatic nucleus alters timing of hibernation in ground squirrels.

Hibernation patterns were monitored continuously for 2.5 years in female squirrels that were neurologically intact or in which the hypothalamic suprachiasmatic nucleus (SCN) was completely ablated (SCNx). The number of hibernation bouts in SCNx squirrels increased by 159%, total hibernation time increased by 58%, and periodic arousals from hibernation were 47% longer in SCNx than in control squirrels; the duration of individual torpor bouts was 2 days shorter and far more variable in SCNx than in control animals. Some SCNx squirrels cycled through bouts of torpor continuously for nearly 2 years. The SCN appears to be part of the mechanism that controls the duration of the hibernation season and the temporal structure of individual torpor bouts.

Animals↗

PubMed2000

Expression of polysialic acid, alpha- and beta-cantenins in adult toad testis in hibernation stage and after gonadotrophin--releasing hormone (GnRH) treatment.

The Polysialic Acid (PSA), glycosydic moiety of the Neural Cell Adhesion Molecule (N-CAM), and alpha- and beta-Catenins, which mediate interaction between Cadherins and cytoskeletal proteins, participate in cell adhesion phenomena in numerous organs and tissues. We have performed an immunohistochemical analysis, in hibernating toad testis and in GnRH-reactivated hibernating animals. In hibernating toads we could demonstrate PSA-immunoreactivity (PSA-IR) within the seminiferous tubules, in clusters of primary spermatocytes, spermatids and spermatozoa, in follicular and Sertoli cells. PSA-IR was seen in peritubular, Leydig and efferent duct cells. In GnRH-treated toads PSA-IR persists in primary spermatocyte groups. alpha-Catenin is localized in the basal laminae of seminiferous tubules and in Leydig cells of hibernating toads. This did not change after hormonal treatment. In hibernating toads, beta-Catenin was detected only in Leydig cells and within seminiferous tubules on basal spermatocystes and limiting spermatozoa clusters. In GnRH-treated toads, the beta-Catenin-IR was less intense in Leydig cells and vanished within seminiferous tubules.

Animals↗

PubMed1999

Preparing for inactivity: how insectivorous bats deposit a fat store for hibernation.

During late autumn insectivorous bats must deposit a fat store to cover their energy demands throughout the period of hibernation, yet the density of aerial insects by this time has already declined from its peak in midsummer. Krzanowski (1961) suggested that bats are able to deposit a fat store by manipulating their energy expenditure; specifically by selecting cold roosting locations rather than warm roosts, and depressing their body temperatures during the day roosting period. It was hypothesized that these behavioural changes result in very low daily energy demands, and despite reduced food intake the animals are still able to gain body fat. We made several tests of this hypothesis. First, we explored the thermo-selection behaviour of long-eared bats (Plecotus auritus) in the summer and in the pre-hibernal period. We found that in summer bats preferred temperatures of about 32-35 degrees (about thermoneutral), but in the pre-hibernal period they preferred much colder temperatures of about 10 degrees. Second, using open-flow respirometry we found that in the cold pre-hibernal bats entered torpor for an average of 14 h each day. Compared with bats held at 30 degrees (that did not go torpid), the bats at 7 degrees expended less energy. The extent of saving was sufficient to positively affect their mass balance, despite the fact that bats at lower temperature also had reduced digestive efficiencies. Our findings support the hypothesis that during the pre-hibernal period insectivorous bats manipulate their mass balance primarily by alterations in their energy expenditure, specifically utilizing energy-sparing mechanisms such as torpor.

Adipose Tissue↗

PubMedDate not supplied

Reversible depression of oxygen consumption in isolated liver mitochondria during hibernation.

The biochemical mechanisms by which hibernators cool as they enter torpor are not fully understood. In order to examine whether rates of substrate oxidation vary as a function of hibernation, liver mitochondria were isolated from telemetered ground squirrels (Spermophilus lateralis) in five phases of their annual hibernation cycle: summer active, and torpid, interbout aroused, entrance, and arousing hibernators. Rates of state 3 and state 4 respiration were measured in vitro at 25 degrees C. Relative to mitochondria from summer-active animals, rates of state 3 respiration were significantly depressed in mitochondria from torpid animals yet fully restored during interbout arousals. These findings indicate that a depression of ADP-dependent respiration in liver mitochondria occurs during torpor and is reversed during the interbout arousals to euthermia. Because this inhibition was determined to be temporally independent of entrance and arousal, it is unlikely that active suppression of state 3 respiration causes entrance into torpor by facilitating metabolic depression. In contrast to the observed depression of state 3 respiration in torpid animals, state 4 respiration did not differ significantly among any of the five groups, suggesting that alterations in proton leak are not contributing appreciably to downregulation of respiration in hibernation.

Animals↗

PubMedDate not supplied

The effects of caloric restriction on the body composition and hibernation of the golden-mantled ground squirrel (Spermophilus lateralis).

In preparation for hibernation, golden-mantled ground squirrels (Spermophilus lateralis) must deposit sufficient amounts of lipid during the summer to survive winter hibernation. We conducted an experiment from May 1998 to February 1999 to examine the effects of caloric restriction on the body composition (lipid and fat-free mass) and hibernation of golden-mantled ground squirrels. Ground squirrels were either provided with food ad lib. (controls) or with only enough food to maintain a constant body mass throughout the experiment (calorically restricted). Changes in body composition were followed using total body electrical conductivity (TOBEC). Implanted data loggers that recorded body temperature were used to determine when ground squirrels entered their first torpor bout and the lengths of torpor bouts. Body composition did not change in the calorically restricted ground squirrels between May and September, while both lipid and fat-free mass increased in the controls. However, from September to February, calorically restricted ground squirrels lost only fat-free mass, not lipid mass, but controls lost both lipid and fat-free mass. Calorically restricted ground squirrels entered their first torpor bout about 4 wk after controls, but the torpor bout duration (or length) during hibernation did not differ between the two groups. These results show that ground squirrels maintain body composition during caloric restriction, and the limited quantities of stored lipid have an effect on when hibernation begins but not on torpor bout length.

Animals↗