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PubMed2006

Persistent tolerance to oxygen and nutrient deprivation and N-methyl-D-aspartate in cultured hippocampal slices from hibernating Arctic ground squirrel.

Hibernating Arctic ground squirrel (hAGS), Spermophilus parryii, survive profound decreases in cerebral perfusion during torpor and return to normal blood flow during intermittent rewarming periods without neurologic damage. Hibernating AGS tolerate traumatic brain injury in vivo, and acute hippocampal slices from hibernating animals tolerate oxygen and glucose deprivation. It remains unclear, however, if neuroprotection results from intrinsic tissue properties or from differences in response to acute trauma associated with slice preparation. The goal of this work was therefore to determine whether an intrinsic tissue tolerance persists in chronic culture of AGS hippocampal slices at 37 degrees C. A second goal was to address N-methyl-D-aspartate (NMDA) receptor involvement and channel arrest as potential mechanisms of intrinsic tissue tolerance. Baseline neuronal survival and tolerance to oxygen and nutrient deprivation (OND), an in vitro model of ischemia-reperfusion, were assessed in the CA1 region of hippocampal slices from juvenile, hAGS and interbout euthermic AGS (ibeAGS). Early in culture (insult onset at 3 h), slices from both hAGS and ibeAGS tolerate OND (4 h deprivation followed by 20 h recovery) and 500 micromol/L NMDA plus 20 mmol/L KCl. Later in culture (insult onset at 24 h), tolerance persists in slices from hAGS but not in slices from ibeAGS. Ouabain (Na(+)K(+)ATPase inhibitor) administered 24 h in culture enhances survival of slices from hAGS (assessed 24 h later). Thus, tolerance to OND in slices from hAGS is due to intrinsic tissue properties likely involving NMDA receptors and ion channel arrest.

Animals↗
PubMed2006

Protein SUMOylation is massively increased in hibernation torpor and is critical for the cytoprotection provided by ischemic preconditioning and hypothermia in SHSY5Y cells.

Hibernation torpor provides an excellent natural model of tolerance to profound reductions in blood flow to the brain and other organs. Here, we report that during torpor of 13-lined ground squirrels, massive SUMOylation occurs in the brain, liver, and kidney. The level of small ubiquitin-related modifier (SUMO) conjugation coincides with the expression level of Ubc9, the SUMO specific E2-conjugating enzyme. Hypothermia alone also increased SUMO conjugation, but not as markedly as hibernation torpor. Increased SUMO conjugation (induced by Ubc9 overexpression, ischemic preconditioning (PC)+/-hypothermia) was necessary and sufficient for tolerance of SHSY5Y neuroblastoma cells to oxygen/glucose deprivation (OGD) ('in vitro ischemia'); decreased SUMO conjugation (induced by a dominant-negative Ubc9) severely reduced tolerance to OGD in these cells. These data indicate that post-translational modification of proteins by SUMOylation is a prominent feature of hibernation torpor and is critical for cytoprotection by ischemic PC+/-hypothermia in SHSY5Y cells subjected to OGD.

Animals↗
PubMed1982

Extracts from the brains of hibernating and alert ground squirrels: effects on cells in culture.

Aqueous extracts were prepared from pulverized, acetone-dehydrated brains of hibernating and alert ground squirrels. Addition of these extracts to Chinese hamster ovary cells in suspension culture resulted in a decrease in the amount of [3H]thymidine incorporated into acid-precipitable material without affecting the transport or phosphorylation of the nucleoside. The inhibition was time- and dose-dependent and full recovery occurred about 2 hr after exposure of the cells to the active extract. The active factor is readily oxidized during storage at -70 degrees C but full activity can be restored by treatment with 2-mercaptoethanol. The peptide nature of the active material is indicated by its susceptibility to proteases and by loss of activity after alkylation. Fasted or cold-acclimated rats also develop increased levels of active substance in their brains; however, brains of hibernating squirrels contain 10- to 50-fold more of the active substance than brains from either alert squirrels or rats. A time-dependent increase in activity of extracts from hibernating brain incubated with a homogenate from alert brain suggests that the peptide is activated or generated in the mixture.

Animals↗
PubMed2000

Climate change is affecting altitudinal migrants and hibernating species.

Calendar date of the beginning of the growing season at high altitude in the Colorado Rocky Mountains is variable but has not changed significantly over the past 25 years. This result differs from growing evidence from low altitudes that climate change is resulting in a longer growing season, earlier migrations, and earlier reproduction in a variety of taxa. At our study site, the beginning of the growing season is controlled by melting of the previous winter's snowpack. Despite a trend for warmer spring temperatures the average date of snowmelt has not changed, perhaps because of the trend for increased winter precipitation. This disjunction between phenology at low and high altitudes may create problems for species, such as many birds, that migrate over altitudinal gradients. We present data indicating that this already may be true for American robins, which are arriving 14 days earlier than they did in 1981; the interval between arrival date and the first date of bare ground has grown by 18 days. We also report evidence for an effect of climate change on hibernation behavior; yellow-bellied marmots are emerging 38 days earlier than 23 years ago, apparently in response to warmer spring air temperatures. Migrants and hibernators may experience problems as a consequence of these changes in phenology, which may be exacerbated if climate models are correct in their predictions of increased winter snowfall in our study area. The trends we report for earlier formation of permanent snowpack and for a longer period of snow cover also have implications for hibernating species.

Altitude↗
PubMed2004

Quantitative analysis of liver protein expression during hibernation in the golden-mantled ground squirrel.

Mammals that enter deep hibernation experience extreme reductions in body temperature and in metabolic, respiratory, and heart rates for several weeks at a time. Survival of these extremes likely entails a highly regulated network of tissue- and time-specific gene expression patterns that remain largely unknown. To date, studies to identify differentially-expressed genes have employed a candidate gene approach or in a few cases broader unbiased screens at the RNA level. Here we use a proteomic approach to compare and identify differentially expressed liver proteins from two seasonal stages in the golden-mantled ground squirrel (summer and entrance into torpor) using two-dimensional gels followed by MS/MS. Eighty-four two-dimensional gel spots were found that quantitatively alter with the hibernation season, 68 of which gave unambiguous identifications based on similarity to sequences in the available mammalian database. Based on what is known of these proteins from prior research, they are involved in a variety of cellular processes including protein turnover, detoxification, purine biosynthesis, gluconeogenesis, lipid metabolism and mobility, ketone body formation, cell structure, and redox balance. A number of the enzymes found to change seasonally are known to be either rate-limiting or first enzymes in a metabolic pathway, indicating key roles in metabolic control. Functional roles are proposed to explain the changes seen in protein levels and their potential influence on the phenotype of hibernation.

Amino Acid Sequence↗
PubMed1996

An ultrastructural and cytochemical study of the mesonephros of Rana esculenta during activity and hibernation.

The biological cycle of most amphibians undergoes seasonal variations. In this study, we investigated the mesonephros of Rana esculenta during active life and the natural hibernation period. The ultrastructural morphology of the different tracts constituting the nephron was analysed. Moreover, to evaluate the effect of seasonal temperature variations on the mesonephros function, the activity of some enzymes linked to membrane transport and playing regulatory roles in various metabolic pathways was investigated in different tracts of the frog nephron. During hibernation the glomerular filtration barrier appeared thicker than in the active life, lysosomes and paraplasmatic material, mostly glycogen, being accumulated in the proximal and distal tubule cells respectively. Cytoplasmic organelles, i.e., mitochondria, endoplasmic reticulum were observed in segregated areas. At the same time, changes in some enzyme activities were noted. The activity of some membrane-transport enzymes (5' nucleotidase and K+-p-nitrophenyl phosphatase) and of energetic metabolism (succinic dehydrogenase) was reduced. Nevertheless the alkaline phosphatase activity was not changed significantly, and this suggests that some metabolic activities were preserved in the hibernating samples. These results indicate morpho-functional adaptations of the kidney cells that preserve their role in osmoregulation and some metabolic processes, even during unfavourable seasons.

4-Nitrophenylphosphatase↗
PubMedDate not supplied

Lactation during hibernation in wild black bears: effects on plasma amino acids and nitrogen metabolites.

This study examined the seasonal and reproductive influences on individual plasma amino acid concentrations and nitrogen metabolites in a black bear population (Ontario, Canada). During hibernation, 11 of 23 plasma amino acids were significantly higher (13%-108%) in lactating than in nonlactating females, without an alteration in plasma total protein or total essential or nonessential amino acid levels. The greatest changes were observed in glutamine, arginine, and glycine levels. Plasma urea, urea/creatinine, and ammonia levels were significantly lower in hibernating compared with active female bears, but lactation had no effect on these parameters. Taken together these results show that lactation during hibernation is an additional metabolic challenge that results in increased mobilization of individual plasma amino acids and no accumulation of nitrogen end products, underlining the remarkable efficiency of amino acid and urea recycling in denning female black bears.

Amino Acids↗
PubMedDate not supplied

Torpor and digestion in food-storing hibernators.

Many species of hibernating mammals rely on hoarded food rather than body fat to support winter energy requirements. Here, we evaluate whether the associated ingestive and digestive requirements reduce the benefits that food-storing hibernators can accrue from torpor. Using a simple model, we predict (1) that digestive efficiency could either increase or decrease with increased use of torpor, depending on the Q(10) of digestion relative to the Q(10) of whole-animal metabolism and (2) that increased torpor will result in a linear decrease in energy consumption but an exponential increase in euthermic intake requirements. In 16 captive eastern chipmunks (Tamias striatus), the proportion of time that different individuals spent in torpor was highly variable (29.8%+/-5.9%; 0.0%-86.3%), positively correlated with dry matter digestibility (r2=0.53, P=0.02) and negatively correlated with energy consumption (r2=0.72, P=0.002). Thus, by both increasing conversion efficiency and reducing energy requirements, torpor appears to provide a double benefit for energy conservation by food-storing hibernators. Despite this, a comparative analysis shows that the euthermic intervals of food-storing rodents are four times as long and torpor intervals are half as long as that of fat-storing rodents. Given that required euthermic intake rates are expected to increase exponentially at high levels of torpor, the reduced torpor expression of food-storing species may result from constraints on their ability to load enough food into the gut when euthermic to cover the energy requirements of the subsequent torpor cycle.

Animals↗
PubMedDate not supplied

Aerobic capacity of frog skeletal muscle during hibernation.

Frogs submerged at 3 degrees C in hypoxic water (Po2=60 mmHg) depress their metabolic rate to 25% of that seen in control animals with access to air. The hypometabolic state of the skeletal muscle in such cold-submerged frogs is thought to be the most important contributor to the overall metabolic depression. The aim of this study was to determine whether the aerobic capacity of frog skeletal muscle became altered during 1-4 mo of hibernation to match the reduction in adenosine triphosphate (ATP) demand. To this end, the activities of key mitochondrial enzymes were measured in the skeletal muscle and in isolated mitochondria of frogs at different stages during hibernation. We also measured the activity of lactate dehydrogenase (LDH) as an indicator of glycolytic capacity. The activities of cytochrome c oxidase, citrate synthase, and LDH were significantly lower in frog skeletal muscle after 4 mo of hibernation compared with control conditions. The reduction in skeletal muscle aerobic capacity is apparently due to changes in the intrinsic properties of the mitochondria. Overall, these results indicate an important reorganisation of ATP-producing pathways during long-term metabolic depression to match the lowered ATP demand.

Aerobiosis↗
PubMed1976

Hibernation and circannual rhythms of food consumption in marmots and ground squirrels.

In order to understand better the evolution and adaptive value of hibernation, ecological aspects and experimental studies of closely related hibernators, the Marmotini, are examined. The central hypothesis is that annual changes in the environment integrate three or, perhaps, four physiological processes: torpor, reporduction, consumption of food, and metabolism. Reproduction occurs promptly after emergence from hibernation. For most species, the breeding season is very short. Although the experimental data are rather meager, no variation in external factors has consistently altered the season of reproduction. Consumption of food and change in weight increases until July or September and then decreases. The large members of the Marmotini store their energy as fat, but small species store their energy as seeds and nuts. Experiments to test the hypothesis that some aspect of the supply, such as fat content, might vary seasonally have produced negative results. Complex experiments on the length of the photoperiod on woodchucks and several species of ground squirrels failed to alter the annual cycle of consumption of food. Animals kept in constant conditions showed a cycle of about 11 months, but woodchucks sent tto Australia changed their cycle in two years to match the seasons of the southern hemisphere. Experiments with temperature and torpor and castration did not alter the annual did not alter the rhythm...

Adipose Tissue↗
PubMed1986

Pineal melatonin rhythms in female Turkish hamsters: effects of photoperiod and hibernation.

Daily rhythms of pineal and serum melatonin content were characterized for adult female Turkish hamsters (Mesocricetus brandti) exposed to long days (16L:8D, 22 degrees C) or after transfer to short days (10L:14D, 22 degrees C). The nocturnal peak of pineal melatonin content was found to be approximately 3 b greater in duration on short than on long days. Changes in levels of serum melatonin closely paralleled those of pineal melatonin. Thus, an effect of photoperiod on synthesis and secretion of pineal melatonin was demonstrated. In a separate experiment, female hamsters were induced to hibernate by exposure to a short-day, cold environment (10L:14D, 6 degrees C). During the 4 to 5-mo hibernation season, Turkish hamsters are known to display 4 to 8-day hours of torpor (body temperature = 7-9 degrees C) alternating with 1 to 3-day intervals of euthermia (body temperature = 35-37 degrees C). Little evidence of nocturnal synthesis or secretion of pineal melatonin was detected in females sampled during torpor. However, animals sampled during the first day after arousal from a torpor bout displayed melatonin rhythms no different in phase or amplitude from those seen in females held at 22 degrees C. Thus, despite the absence of pineal melatonin output during torpor, the pineal gland of hibernating Turkish hamsters produces an appropriately phased, rhythmic melatonin signal during intervals of euthermia.

Aging↗
PubMed2003

Serum markers of bone metabolism show bone loss in hibernating bears.

Disuse osteopenia was studied in hibernating black bears (Ursus americanus) using serum markers of bone metabolism. Blood samples were collected from male and female, wild black bears during winter denning and active summer periods. Radioimmunoassays were done to determine serum concentrations of cortisol, the carboxy-terminal cross-linked telopeptide, and the carboxy-terminal propeptide of Type I procollagen, which are markers of bone resorption and formation, respectively. The bone resorption marker was significantly higher during winter hibernation than it was in the active summer months, but the bone formation marker was unchanged, suggesting an imbalance in bone remodeling and a net bone loss during disuse. Serum cortisol was significantly correlated with the bone resorption marker, but not with the bone formation marker. The bone formation marker was four- to fivefold higher in an adolescent and a 17-year-old bear early in the remobilization period compared with the later summer months. These findings raise the possibility that hibernating black bears may minimize bone loss during disuse by maintaining osteoblastic function and have a more efficient compensatory mechanism for recovering immobilization-induced bone loss than that of humans or other animals.

Animals↗
PubMed2006

delta-Opioid-induced pharmacologic myocardial hibernation during cardiopulmonary resuscitation.

OBJECTIVES: Cardiac arrest and cardiopulmonary resuscitation is an event of global myocardial ischemia and reperfusion, which is associated with severe postresuscitation myocardial dysfunction and fatal outcome. Evidence has demonstrated that mammalian hibernation is triggered by cyclic variation of a delta-opiate-like compound in endogenous serum, during which the myocardial metabolism is dramatically reduced and the myocardium tolerates the stress of ischemia and reperfusion without overt ischemic and reperfusion injury. Previous investigations also proved that the delta-opioid agonist elicited the cardioprotection in a model of regional ischemic intact heart or myocyte. Accordingly, we were prompted to search for an alternative intervention of pharmacologically induced myocardial hibernation that would result in rapid reductions of myocardial metabolism and therefore minimize the myocardial ischemic and reperfusion injury during cardiac arrest and cardiopulmonary resuscitation. DESIGN: Prospective, controlled laboratory study. SETTING: University-affiliated research laboratory. INTERVENTIONS: In the series of studies performed in the established rat and pig model of cardiac arrest and cardiopulmonary resuscitation, the delta-opioid receptor agonist, pentazocine, was administered during ventricular fibrillation. MEASUREMENTS AND MAIN RESULTS: : The myocardial metabolism reflected by the concentration of lactate, or myocardial tissue PCO2 and PO2, is dramatically reduced during cardiac arrest and cardiopulmonary resuscitation. These are associated with less severe postresuscitation myocardial dysfunction and longer duration of postresuscitation survival. CONCLUSIONS: delta-Opioid-induced pharmacologic myocardial hibernation is an option to minimize the myocardial ischemia and reperfusion injury during cardiac arrest and cardiopulmonary resuscitation.

Animals↗
PubMed1998

Evolution of daily torpor and hibernation in birds and mammals: importance of body size.

1. The evolution of hibernation and daily torpor in mammals and birds remains a controversial subject. The original view was that use of torpor reflects a primitive thermoregulation, as it occurs in ancestral groups of mammals. 2. This view is no longer widely supported. However, the interpretation of a polyphyletic derivation of torpor also has been challenged because of the astonishing similarity of torpor patterns among various orders and even the two classes. 3. A recent argument is that mutations required for torpor and hibernation are unlikely to occur simultaneously and that torpor must be plesiomorphic (ancestral), although it is not functionally primitive. Homeothermy is interpreted as a loss of the ability to enter torpor in those groups that could survive without the requirement of heterothermic periods for energy conservation. 4. Interestingly, while torpor in mammals occurs in the phylogenetically old groups, lending support to the hypothesis of an ancestral derivation of torpor, the opposite is the case for birds. Modern bird groups and ancestral mammal groups contain mainly small species that often rely on fluctuating food supply, whereas modern mammalian orders and ancient bird orders contain the largest species with low energy requirements for maintenance and thermoregulation. 5. It is, therefore, possible that not phylogenetic position but size and diet determine the occurrence of heterothermy. Moreover, because endothermy and torpor in birds has apparently evolved separately from that in mammals and because it is possible that daily torpor and hibernation represent two distinct torpor patterns that evolved separately, a convergent evolution of torpor in endotherms cannot be excluded.

Animals↗
PubMed1988

Comparison between effects of caffeine and ryanodine on electromechanical coupling in myocardium of hibernating chipmunks: role of internal Ca stores.

1. To clarify the cause of uncoupling of Ca influx through Ca channels and the contractility of the myocardium in hibernating chipmunks, the electromechanical effects of two different internal Ca store inhibitors, caffeine and ryanodine, and a cardiotonic agent, isoprenaline, were investigated in papillary muscles of hibernating animals. 2. Ryanodine (10(-6) M), an inhibitor of internal Ca release, abolished the contraction with a marked inhibition of the action potential plateau (APp). In such preparations, an increase in Ca influx induced by isoprenaline (5 x 10(-8) M) failed to augment the contraction, indicating uncoupling of Ca influx and contraction. 3. In ryanodine pretreated preparations, 10 mM caffeine produced an early phase of APp, but did not affect the contraction abolished by ryanodine, while a higher concentration of caffeine (25 mM) markedly increased the contraction with an augmentation of the electrical response. 4. In the absence of ryanodine, caffeine (5 mM) almost abolished the contraction with a greater inhibition of APp. In such preparations, isoprenaline greatly increased the contraction with an augmentation of the early phase of APp. 5. These effects were not significantly affected by additional application of ryanodine, but were inhibited by nifedipine, a Ca channel blocker. 6. These observations suggest that in cardiac muscles of hibernating animals, lack of the positive inotropic effect of isoprenaline may be attributed to a rapid and effective sequestration of increased cytoplasmic Ca through Ca influx by internal stores, probably by enhancement of their ability to take up Ca.

Action Potentials↗
PubMed1989

Freeze avoidance in a mammal: body temperatures below 0 degree C in an Arctic hibernator.

Hibernating arctic ground squirrels, Spermophilus parryii, were able to adopt and spontaneously arouse from core body temperatures as low as -2.9 degrees C without freezing. Abdominal body temperatures of ground squirrels hibernating in outdoor burrows were recorded with temperature-sensitive radiotransmitter implants. Body temperatures and soil temperatures at hibernaculum depth reached average minima during February of -1.9 degrees and -6 degrees C, respectively. Laboratory-housed ground squirrels hibernating in ambient temperatures of -4.3 degrees C maintained above 0 degree C thoracic temperatures but decreased colonic temperatures to as low as -1.3 degrees C. Plasma sampled from animals with below 0 degree C body temperatures had normal solute concentrations and showed no evidence of containing antifreeze molecules.

Animals↗
PubMed1981

Physical dependence on morphine fails to develop during the hibernating state.

Physical dependence on morphine occurs in a typical fashion during the active state of the mammalian hibernator Citellus lateralis, but does not occur when morphine exposure is confined to the hibernating state. Morphine exposure during hibernation can produce stereotyped behavior, thus demonstrating partial responsiveness of the central nervous system to opioids during this natural state.

Animals↗
PubMed1977

Hibernation and body weight in dormice: a new type of endogenous cycle.

Under conditions unfavorable to hibernateion (22 degrees C), the body-weight cycles of dormice are only a few weeks long, but under conditions in which dormice hibernate (5 degrees C), the cycles can last many months; the more the animals hibernate, the longer are the cycles. Such cycles contrast with the relative independence from torpor of the period of circannual cycles in other hibernating rodents and with the temperature compensation of circannual and circadian cycles in general.

Animals↗