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PubMed2006

Hibernation confers resistance to intestinal ischemia-reperfusion injury.

The damaging effects of intestinal ischemia-reperfusion (I/R) on the gut and remote organs can be attenuated by subjecting the intestine to a prior, less severe I/R insult, a process known as preconditioning. Because intestines of hibernating ground squirrels experience repeated cycles of hypoperfusion and reperfusion, we examined whether hibernation serves as a model for natural preconditioning against I/R-induced injury. We induced intestinal I/R in either the entire gut or in isolated intestinal loops using rats, summer ground squirrels, and hibernating squirrels during natural interbout arousals (IBA; body temperature 37-39 degrees C). In both models, I/R induced less mucosal damage in IBA squirrels than in summer squirrels or rats. Superior mesenteric artery I/R increased MPO activity in the gut mucosa and lung of rats and summer squirrels and the liver of rats but had no effect in IBA squirrels. I/R in isolated loops increased luminal albumin levels, suggesting increased gut permeability in rats and summer squirrels but not IBA squirrels. The results suggest that the hibernation phenotype is associated with natural protection against intestinal I/R injury.

Animals↗
PubMed2004

Insights into cardioprotection obtained from study of cellular Ca2+ handling in myocardium of true hibernating mammals.

Mammalian hibernators exhibit remarkable resistance to low body temperature, whereas non-hibernating (NHB) mammals develop ventricular dysfunction and arrhythmias. To investigate this adaptive change, we compared contractile and electrophysiological properties of left ventricular myocytes isolated from hibernating (HB) woodchucks (Marmota monax) and control NHB woodchucks. The major findings of this study were the following: 1) the action potential duration in HB myocytes was significantly shorter than in NHB myocytes, but the amplitude of peak contraction was unchanged; 2) HB myocytes had a 33% decreased L-type Ca2+ current (I(Ca)) density and twofold faster I(Ca) inactivation but no change in the current-voltage relationship; 3) there were no changes in the density of inward rectifier K+ current, transient outward K+ current, or Na+/Ca2+ exchange current, but HB myocytes had increased sarcoplasmic reticulum Ca2+ content as estimated from caffeine-induced Na+/Ca2+ exchange current values; 4) expression of the L-type Ca2+ channel alpha(1C)-subunit was decreased by 30% in HB hearts; and 5) mRNA and protein levels of sarco(endo)plasmic reticulum Ca2+-ATPase 2a (SERCA2a), phospholamban, and the Na+/Ca2+ exchanger showed a pattern that is consistent with functional measurements: SERCA2a was increased and phospholamban was decreased in HB relative to NHB hearts with no change in the Na+/Ca2+ exchanger. Thus reduced Ca2+ channel density and faster I(Ca) inactivation coupled to enhanced sarcoplasmic reticulum Ca2+ release may underlie shorter action potentials with sustained contractility in HB hearts. These changes may account for natural resistance to Ca2+ overload-related ventricular dysfunction and point to an important cardioprotective mechanism during true hibernation.

Action Potentials↗
PubMed1975

Concentration of urine by the hibernating marmot.

Studies wer performed with marmots (Marmota flaviventris) of both sexes that had chronic arterial, venous, and bladder catheters. Urine collection was performed during hibernation and urine osmolalities (611.6 not equal to 166.1 SD) were found to be lower than those of aroused animals (1264 not equal to 472.9 SD), but hypertonic to plasma. Peak osmolality of meduallary slices was found to be in the range of osmotic pressures of urine obtained from hibernating or aroused animals. After single injections of a mixture of rho-aminohippurate and inulin, or during constant infusion of inulin, steady-state excretion by hibernators was not achieved for several days. Indirect evidence indicateds that the hibernating marmot is capable of PAH secretion.

Aminohippuric Acids↗
PubMed2005

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

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 O2 saturation (S(O2), and indexes of cellular and physiological stress were measured during hibernation and euthermy and after arousal thermogenesis. Results show that arterial O2 tension (Pa(O2)) and S(O2) are severely diminished during arousal and that hypoxia-inducible factor (HIF)-1alpha 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 S(O2) and accumulation of HIF-1alpha 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.

Adaptation, Physiological↗
PubMed1977

Sleep and hibernation in ground squirrels (Citellus spp): electrophysiological observations.

Electroencephalogram (EEG), electrooculogram, electromyogram, and electrocardiogram were recorded from ground squirrels (Citellus beldingi and C. lateralis) during the summer and also during the hibernation season. Summer recordings revealed that the animals spent an average of 66% of the 24-h period asleep (49% of the 12-h light period and 84% of the 12-h dark period); 19% of the total sleep time (TST) consisted of rapid-eye-movement (REM) sleep, and 81% of TST consisted of slow-wave sleep (SWS). Recordings obtained during the hibernation season showed that hibernation was entered through sleep, but the distribution of sleep states was different than in euthermic sleep. During the early entrance when brain temperature (Tbr) was between 35 and 25 degrees C, the animals were asleep 88% of the time, but only 10% of the TST was spent in REM sleep. The EEG amplitude declined with decreased Tbr so that classical sleep stages could not be identified below a Tbr of 25 degrees C. The frequency of the EEG increased as Tbr decreased; but activity in the 0-4 cycles/s band occupied the majority of the record even at a Tbr of 10 degrees C. Below a Tbr of 10 degrees C the EEG was isoelectric except for intermittent bursts of spindles. It was concluded from these and other results that the entrance into hibernation represents an extension of the thermoregulatory adjustments that occur during SWS.

Animals↗
PubMed1985

Ketone body metabolism in a ground squirrel during hibernation and fasting.

Hibernating Belding's ground squirrels (Spermophilus beldingi) are ketotic relative to fed nonhibernators. Muscles from torpid individuals, when incubated in media containing physiological concentrations of glucose and ketone, show reduced uptake of glucose in the presence of ketone. The magnitude of the reduction is dependent on ketone concentration and reaches 60% in heart and 100% in pectoralis at 1.4 mM ketone. Fasted squirrels are also ketotic. However, ketone does not reduce glucose uptake in muscles from fed or fasted animals. Glucose utilization by muscles decreases during a long-term fast, but the reduction is independent of ketone. Thus both a long-term fast and hibernation lead to changes in muscle tissues that decrease their reliance on glucose as an energy source. Ketosis leads to glucose sparing during hibernation, whereas muscle glucose utilization is decreased independently of ketone during a fast. The glucose sparing achieved in both hibernation and fasting leads to conservation of body protein, the major source of gluconeogenic precursors in fasting mammals.

Animals↗
PubMed1986

Does serotonin play a role in entrance into hibernation?

To study the role of brain serotonin in entrance into hibernation, intraventricular injections of 5,7-dihydroxytryptamine, electrolytic lesions of small parts of the median raphe nucleus, and chemical lesions of the same nucleus were undertaken on the European hamster in winter. All the lesions led to a variable decrease of serotonin levels in all parts of the brain areas examined. However, hibernation was suppressed only in those animals whose serotonergic neurons were destroyed in a small anterior part of the median raphe nucleus. Electrolytic lesions as well as chemical lesions in the other parts of the median raphe nucleus or the 5,7-dihydroxytryptamine injections into lateral ventricles do not prevent hibernation. These data suggest that in the European hamster only a specific group of serotonergic neurons of the median raphe nucleus are involved in the process of entrance into hibernation.

5,7-Dihydroxytryptamine↗
PubMed1988

Progressive activation of paratrigeminal nucleus during entrance to hibernation.

The paratrigeminal nucleus (Pa5) undergoes a progressive increase in its uptake of 2-[14C]deoxyglucose (2DG) relative to other brain structures during entrance to hibernation in the ground squirrel. This highly significant increase results in the Pa5 becoming the most highly labeled brain region during hibernation, even though it exhibits one of the lowest levels of 2DG uptake in the brain during the nonhibernating state. The progressive activation of the Pa5 observed during entrance is reversed during arousal from hibernation. These observations and the neuroanatomical projections of the Pa5 implicate this nucleus as playing a role in the entrance and maintenance of the hibernating state.

Animals↗
PubMed1989

Suprachiasmatic nucleus: phase-dependent activation during the hibernation cycle.

The suprachiasmatic nucleus (SCN) of the golden-mantled ground squirrel undergoes a phase-dependent change in its accumulation of 2-[14C]deoxy-D-glucose (2-DG) relative to other brain structures during the hibernation cycle. The greatest relative 2-DG uptake (R2DGU) is observed in the SCN during entrance into and during deep hibernation. A circadian fluctuation in R2DGU of the SCN is not evident in the euthermic ground squirrel but can be increased during the subjective day by photic stimulation. An increase in R2DGU by the paraventricular nucleus (PVN) correlates with the increase in R2DGU by the SCN during entrance to hibernation but not with the increase in SCN R2DGU evoked by photic stimulation during euthermia. The periventricular nuclei of the hypothalamus (PEV) also have high levels of R2DGU during the latter phase of the entrance. These observations support the hypothesis that the SCN, PEV, and PVN may play important roles in hibernation and suggest progressive activation of synaptic input to and within the SCN during entrance into this state.

Animals↗
PubMed1991

Disuse atrophy in the hibernating golden-mantled ground squirrel, Spermophilus lateralis.

Disuse (inactivity, bed rest, and spaceflight) may lead to a loss of muscle mass and a decrease in oxidative capacity in skeletal muscle. If such changes were to occur in hibernating animals, both locomotor and thermogenic function would be compromised. Muscle masses and oxidative capacities (as assessed by citrate synthase activity) were measured in the gastrocnemius and semitendinosus muscles, cardiac muscle (ventricle), and brown fat (axillary pad) in a group (n = 7) of prehibernating ground squirrels (Spermophilus lateralis) and after 6 mo of hibernation (n = 8). Hibernation produced significant atrophy in the gastrocnemius (14%) and semitendinosus (42%) muscles. Cardiac tissue increased (21%) in mass, as did brown adipose tissue (150%). That such changes were not due simply to fluid shifts was evidenced by similar protein concentrations between groups. In contrast to many other disuse studies, oxidative capacity was increased significantly in the gastrocnemius (65%) and semitendinosus (37%). Citrate synthase was also higher in cardiac tissue of hibernators (20%) but was not significantly different in brown fat.

Adipose Tissue↗
PubMed1993

Adaptations of myocardial beta-adrenergic receptor complex in hibernating marmots.

Properties of marmot (Marmota flaviventris) myocardial beta-adrenergic receptor complex (beta-AR) were evaluated during hibernation (H), in summer (S) animals, and in animals aroused from hibernation (C). The results obtained for S and C animals were identical, and only the results for C animals are shown. In H-animal myocardial membrane preparations assayed at 37 degrees C, isoproterenol-dependent adenylate cyclase activity (ACA) was consistently higher, whereas the synergistic contribution of 5'-guanylylimidodiphosphate [Gpp(NH)p] in this reaction was reduced. When assayed at 10 degrees C, only the ACA in H animals responded to the combination of isoproterenol and Gpp(NH)p. In contrast, at 10 degrees C, ACA in response to Gpp(NH)p alone is essentially equal in H and C animals. Hibernation did not change myocardial beta-AR receptor density or affinity. In contrast, analysis of isoproterenol displacement of [125I]iodocyanopindolol revealed that the proportion of beta-AR in the high-affinity state was substantially greater in H than in C animals, and this relationship was retained even in the presence of Gpp-(NH)p. In an evaluation of the role of the GTP binding proteins that couple the beta-AR to the effector adenyl cyclase, we determined that there was no change in the cholera toxin- or pertussis toxin-dependent ADP ribosylation patterns. Immunochemical detection of the individual GTP binding proteins revealed no change in the levels of G alpha i1, G alpha i2, or G alpha i3. In contrast, we observed a hibernation-associated decrease in G alpha o associated with the plasma membrane-enriched particulate fraction. (ABSTRACT TRUNCATED AT 250 WORDS)

Adaptation, Physiological↗
PubMed1982

Effects of temperature on the duration of arousal episodes during hibernation.

The length of time that the ground squirrels Spermophilus beldingi and S. lateralis remained at high body temperatures following periodic arousals from hibernation increased as environmental temperature increased over the range of 5-20 degree C. This trend was evident in comparisons among different animals that hibernated at different temperatures and in individuals that hibernated at different temperatures in successive years. At any one temperature, the duration of these euthermic intervals in S. beldingi was correlated with body size. Large adult males remained at high body temperatures longer than adult females, which in turn remained euthermic longer than small juveniles. In addition, these squirrels spent less time at high body temperatures following bouts of torpor that were interrupted prematurely by environmental disturbances. These results are consistent with an amplify the theory that arousals are initiated by, and necessary for the elimination of, some chemical imbalance, which develops while hibernators metabolize at low body temperatures.

Animals↗
PubMed2004

Cloning and sequencing of myosin heavy chain isoform cDNAs in golden-mantled ground squirrels: effects of hibernation on mRNA expression.

The golden-mantled ground squirrel is a small rodent hibernator that demonstrates unusual myosin heavy chain (MHC) isoform plasticity during several months of torpor, punctuated by bouts of rewarming and shivering thermogenesis. We measured MHC mRNA levels to determine whether pretranslational control mechanisms were responsible for differences in MHC2x protein expression, as we previously observed between active and hibernating ground squirrels. We first cloned cDNA using the 3' rapid amplification of cDNA ends (3' RACE) technique and identified three sequences corresponding to MHC1, MHC2x, and MHC2b. A DNA control fragment was developed to be used in conjunction with a coupled RT-PCR reaction to simultaneously measure MHC mRNA levels for each isoform in the skeletal muscle of ground squirrels. MHC mRNA and protein expression were strongly correlated, and type IIx and IIb mRNA levels were significantly different between active and hibernating ground squirrels. Pretranslational control of MHC protein is apparently an important process during hibernation, although the exact stimulus is not known. The techniques presented can be used to obtain MHC cDNA sequences and to measure mRNA expression in many vertebrate groups.

Animals↗
PubMed2002

Quantitative assessment of ground squirrel mRNA levels in multiple stages of hibernation.

Hibernators in torpor dramatically reduce their metabolic, respiratory, and heart rates and core body temperature. These extreme physiological conditions are frequently and rapidly reversed during the winter hibernation season via endogenous mechanisms. This phenotype must derive from regulated expression of the hibernator's genome; to identify its molecular components, a cDNA subtraction was used to enrich for seasonally upregulated mRNAs in liver of golden-mantled ground squirrels. The relative steady-state levels for seven mRNAs identified by this screen, plus five others, were measured and analyzed for seasonal and stage-specific differences using kinetic RT-PCR. Four mRNAs show seasonal upregulation in which all five winter stages differ significantly from and are higher than summer (alpha2-macroglobulin, apolipoprotein A1, cathepsin H, and thyroxine-binding globulin). One of these mRNAs, alpha2-macroglobulin, varies during the winter stages with significantly lower levels at late torpor. None of the 12 mRNAs increased during torpor. The implications for these newly recognized upregulated mRNAs for hibernation as well as more global issues of maintaining steady-state levels of mRNA during torpor are discussed.

Animals↗
PubMed2002

Coordinate expression of the PDK4 gene: a means of regulating fuel selection in a hibernating mammal.

Hibernation in mammals requires a metabolic shift away from the oxidation of carbohydrates and toward the combustion of stored fatty acids as the primary source of energy during torpor. A key element involved in this fuel selection is pyruvate dehydrogenase kinase isoenzyme 4 (PDK4). PDK4 inhibits pyruvate dehydrogenase and thus minimizes carbohydrate oxidation by preventing the flow of glycolytic products into the tricarboxylic acid cycle. This paper examines expression of the PDK4 gene during hibernation in heart, skeletal muscle, and white adipose tissue (WAT) of the 13-lined ground squirrel, Spermophilus tridecemlineatus. During hibernation PDK4 mRNA levels increase 5-fold in skeletal muscle and 15-fold in WAT compared with summer-active levels. Similarly, PDK4 protein is increased threefold in heart, fivefold in skeletal muscle, and eightfold in WAT. High levels of serum insulin, likely to have an inhibitory effect on PDK4 gene expression, are seen during fall when PDK4 mRNA levels are low. Coordinate upregulation of PDK4 in three distinct tissues suggests a common signal that regulates PDK4 expression and fuel selection during hibernation.

Adipose Tissue↗
PubMed1990

Long-term lithium treatment does not suppress hibernation in European hamsters.

European hamsters were fed LiCl-supplemented food for a long time before, during and after the hibernating season. Long-term administration of LiCl does not suppress hibernation, which occurs normally during the first part of the experiment. Moreover lithium-treated hibernating hamsters tolerate very high plasma lithium levels. This tolerance is not explained. The results are discussed in relation with the recent theories on the similarities between depression, seasonal affective disorder and hibernation.

Animals↗
PubMed1986

Excitation-contraction coupling in myocardium of nonhibernating and hibernating chipmunks: effects of isoprenaline, a high calcium medium, and ryanodine.

The electromechanical responses to isoprenaline and a high calcium medium on cardiac muscles from nonhibernating and hibernating chipmunks were studied in the presence and the absence of ryanodine. In nonhibernating animal preparations, isoprenaline (5 X 10(-8) M) caused a marked positive inotropic effect with an increase in the amplitude of the action potential plateau and augmented the slow action potential in muscle depolarized with 26 mM K+. In hibernating animal preparations, isoprenaline failed to cause a positive inotropic effect in spite of an increase in the amplitude of action potential plateau and slow action potentials. Similar inotropic effects were caused in the two preparations when extracellular calcium was raised to 6 mM, but action potential plateau and slow action potentials of the two preparations were less affected by this procedure; only in nonhibernating animal preparations was the amplitude of the slow action potential slightly increased. Ryanodine (2 X 10(-6) M) partially inhibited the contraction but augmented the action potential plateau and slow action potentials in nonhibernating animal preparations, while in hibernating animal preparations, it eliminated the contraction and severely inhibited the action potential plateau and slow action potentials. The electrical effects of isoprenaline on the two preparations and of a high calcium medium on nonhibernating animal preparations were more pronounced in the presence of ryanodine than in the absence of it. However, the electrical activity on hibernating animal preparations was unaffected by a high calcium medium in either the presence or absence of ryanodine.(ABSTRACT TRUNCATED AT 250 WORDS)

Action Potentials↗
PubMed2003

Hibernation: when good clocks go cold.

Hibernating animals have been a successful model system for elucidating fundamental properties of many physiological systems. Over the past 50 years, a diverse literature has emerged on the role of the circadian system in control and expression of winter torpor in several orders of birds and mammals. This body of research has also provided insights to circadian function in non-hibernating species. The aim of this review is to examine how this work applies to questions of general interest to chronobiologists, such as temperature compensation, the 2-oscillator model of entrainment, and suprachiasmatic nucleus (SCN) function. Convergent lines of evidence suggest a role for the SCN in timing daily torpor and controlling several parameters of hibernation. In addition to its role as a circadian pacemaker, the SCN may serve a noncircadian function in hibernators related to maintenance of energy balance.

Animals↗