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PubMed2005

Hibernation in the tropics: lessons from a primate.

The Malagasy primate Cheirogaleus medius hibernates in tree holes for 7 months, although ambient temperatures during hibernation rise above 30 degrees C in their natural environment. In a field study we show that during hibernation the body temperature of most lemurs fluctuates between about 10 degrees C and 30 degrees C, closely tracking the diurnal fluctuations of ambient temperature passively. These lemurs do not interrupt hibernation by spontaneous arousals, previously thought to be obligatory for all mammalian hibernators. However, some lemurs hibernate in large trees, which provide better thermal insulation. Their body temperature fluctuates only little around 25 degrees C, but they show regular arousals, as known from temperate and arctic hibernators. The results from this study demonstrate that maximum body temperature is a key factor necessitating the occurrence of arousals. Furthermore, we show that hibernation is not necessarily coupled to low body temperature and, therefore, low body temperature should no longer be included in the definition of hibernation.

Animals↗
PubMed2001

Disassembly of nuclear bodies during arousal from hibernation: an in vitro study.

In previous studies we demonstrated that during hibernation cell nuclei contain structural constituents usually absent in euthermia. The rapid disappearance of such nuclear bodies upon arousal makes very difficult the in vivo investigation of the disassembly process, which could clarify their functions in nuclear metabolism in the hibernator. In the present study we subjected liver samples taken from hibernating edible dormice ( Glis glis) to different in vitro experimental conditions: at 4 degrees C, to preserve the hypothermic state of the hibernating organism; at 37 degrees C, to simulate the drastic increase in body temperature occurring during arousal; at 37 degrees C, in culture medium containing 10(-5) M delta opioid D-Ala2- D-Leu5 enkephalin, which mimics the activity of the hibernation induction trigger in hibernators. Electron microscopic analysis of hepatocyte nuclei at increasing incubation times revealed the subsequent steps of disassembly of coiled bodies, amorphous bodies and fibro-granular material, the unusual structural constituents accumulating during hibernation in these nuclei. We demonstrated that: (1) a temperature of 37 degrees C induces the disappearance of all nuclear bodies typical of hibernation in a few minutes; (2) both low temperature and hibernation-triggering opioid are able to slow down, although to different extents, the process of disassembly of nuclear bodies; (3) the fibro-granular material rapidly disappears during the early phases of incubation; while (4) coiled bodies and amorphous bodies progressively disassemble as fibrous material. Our results support previous hypotheses based on in vivo observations about a possible role for coiled bodies, amorphous bodies and fibro-granular material as storage/assembly sites of molecules needed for the rapid and massive resumption of transcriptional and post-transcriptional activities upon arousal and suggest a strict correlation between the dynamics and metabolic rate of nuclear bodies.

Animals↗
PubMed1996

In vivo microdialysis study on changes in septal dynorphin and beta-endorphin activities in active and hibernating Columbian ground squirrels.

State-dependent changes in extracellular concentration of endogenous opioids in the septum of Columbian ground squirrels were examined in the hibernating and euthermic states using in vivo microdialysis. The order of estimated extracellular concentration was found to be: hibernating > interbout euthermia > non-hibernating euthermia for dynorphin A and interbout euthermia > hibernating > non-hibernating euthermia for beta-endorphin. The apparent turnover rates of dynorphin A during hibernation was 15 times greater than that during euthermic non-hibernation phase and that of beta-endorphin was 8-fold greater. These results demonstrate that subfamilies of endogenous opioids may vary differentially in their activities at different stages of an annual hibernation cycle and may reflect their different roles in the regulation of hibernation.

Animals↗
PubMed1987

Hibernation in garter snakes (Thamnophis sirtalis parietalis): seasonal cycles of cold tolerance.

1. The red-sided garter snake hibernates for about six months each year in Manitoba, Canada, where winter temperatures are often as low as -40 degrees C. Mammalian hibernators typically undergo profound changes in preparation for hibernation, but little is known about corresponding changes in reptiles. 2. We tested the importance of seasonal changes in the ability of red-sided garter snakes to hibernate successfully by exposing them to winter conditions at different times of year. 3. Animals that began hibernation in the fall were more likely to survive hibernation than animals that began hibernation in either early or late summer, despite the fact that the animals were kept on seasonally constant conditions prior to hibernation. 4. We suggest that these changes are derived from endogenous components of the yearly hibernation cycle of red-sided garter snakes but that only part of the cycle proceeds endogenously, i.e. it is not a completely endogenous circannual cycle.

Acclimatization↗
PubMed2004

Up-regulation of fatty acid-binding proteins during hibernation in the little brown bat, Myotis lucifugus.

Hibernating animals rely primarily on lipids throughout winter as their primary fuel source, thus it is hypothesized that an increase in genes and proteins relating to lipid transport will increase accordingly. The cloning and expression of heart type fatty acid-binding protein (h-fabp) from a mammalian hibernator, the little brown bat Myotis lucifugus, is presented. Northern blot analysis revealed that transcript levels of h-fabp were significantly higher during hibernation in brown adipose tissue and skeletal muscle compared with levels in euthermic bats. Similarly, heterologous probing with rat adipose type a-fabp found 3.9-fold higher levels of a-fabp transcripts in brown adipose from hibernating animals. Levels of A- and H-FABP protein were quantified in tissues of euthermic versus hibernating animals by Western blotting. A-FABP was 4-fold higher in brown adipose of hibernating, compared with euthermic bats, whereas H-FABP was significantly higher in hibernator brown adipose, heart and skeletal muscle. The present work implicates FABPs as important elements related to the hibernating state in mammals; alterations in gene and protein expression along with amino acid substitutions are shown. These likely contribute to optimizing the function of FABPs at the low body temperatures (near 0 degrees C) experienced in the hibernating state.

Amino Acid Sequence↗
PubMed2004

Peroxisome proliferator-activated receptors as regulators of lipid metabolism; tissue differential expression in adipose tissues during cold acclimatization and hibernation of jerboa (Jaculus orientalis).

Brown (BAT) and white (WAT) adipose tissues play a key role in the body energy balance orchestrated by the central nervous system. Hibernators have developed a seasonal obesity to respond to inhospitable environment. Jerboa is one of the deep hibernator originated from sub-desert highlands. Thus, this animal represents an excellent model to study cold adaptation mechanism. We report that the adipogenic factor PPARgamma exhibits a differential expression between BAT and WAT at mRNA level. A specific induction was only seen in WAT of pre-hibernating jerboa. Interestingly, PPAR beta/delta is specifically induced in BAT and brain of pre-hibernating jerboa, highlighting for the first time the possible key role of this ubiquitous isoform in the cold adaptation of this true hibernator. Inductions of PPARgamma(2) in WAT and PPAR beta/delta in BAT are blunted by a hypolipemic drug, the ciprofibrate. These changes may be correlated with hibernation arrest and death of treated jerboa. Mitochondrial acyl-CoA dehydrogenase and peroxisomal acyl-CoA oxidase activities in brown and white adipose tissues are decreased up to 85% during cold acclimatization (without food privation). These enzyme activities are subject to a strong induction in BAT and in WAT (3.4-7.5 fold) during the hibernation period. The BAT thermogenesis marker is also largely induced (approximately 4 fold of UCP1 mRNA level) during pre-hibernation period. Unexpectedly, treatment with ciprofibrate deeply affects lipolysis in BAT by increasing acyl-CoA dehydrogenase activity (3.4 fold) and acyl-CoA oxidase at both activity and mRNA levels (2.8 and 3.8 fold, respectively) and enhances strongly UCP1 mRNA level (9.5 fold) during pre-hibernation.

Acclimatization↗
PubMed1997

Use of "natural" hibernation induction triggers for myocardial protection.

BACKGROUND: Hypothermic cardioplegia provides adequate myocellular protection, yet stunning and dysfunction remain significant problems. Interestingly, the subcellular changes of hibernation parallel the altered biology of induced cardiac ischemia, but are well tolerated by hibernating mammalian myocardium. Hibernation induction trigger (HIT) from winter-hibernating animal serum induces hibernation in active animals. Hibernation induction trigger is opiate in nature and is similar to the delta 2 opioids. METHODS: To determine whether HIT could improve myocardial recovery following global ischemia, we gave 37 isolated rabbit hearts either standard cardioplegia or cardioplegia containing summer-active woodchuck, hibernating woodchuck, or black bear HIT serum or a delta 2 opioid, D-Ala2-Leu5-enkephalin, before 2 hours of global ischemia. RESULTS: Hibernation induction trigger appeared not to have an active mechanism during ischemia, as all hearts had equal recovery. In contrast, when examining for a preischemia mechanism, 23 additional rabbits received 3 days pretreatment with summer-active woodchuck or HIT hibernating woodchuck or black bear serum, or were preperfused with D-Ala2-Leu5-enkephalin or D-pen2,5-enkephalin, a-delta 1 opioid, again before 2 hours of global ischemia. Postischemic ventricular function, coronary flows, myocardial oxygen consumption, and ultrastructural preservation were all significantly improved with HIT and D-Ala2-Leu5-enkephalin pretreatment. CONCLUSION: "Natural" HIT protection is superior to standard cardioplegia alone and may have clinical application.

Analysis of Variance↗
PubMed2002

Increased oxidative stress and decreased activities of Ca(2+)/Mg(2+)-ATPase and Na(+)/K(+)-ATPase in the red blood cells of the hibernating black bear.

During hibernation, animals undergo metabolic changes that result in reduced utilization of glucose and oxygen. Fat is known to be the preferential source of energy for hibernating animals. Malonyldialdehyde (MDA) is an end product of fatty acid oxidation, and is generally used as an index of lipid peroxidation. We report here that peroxidation of lipids is increased in the plasma and in the membranes of red blood cells in black bears during hibernation. The plasma MDA content was about four fold higher during hibernation as compared to that during the active, non-hibernating state (P < 0.0001). Similarly, MDA content of erythrocyte membranes was significantly increased during hibernation (P < 0.025). The activity of Ca(2+)/Mg(2+)-ATPase in the erythrocyte membrane was significantly decreased in the hibernating state as compared to the active state. Na(+)/K(+)-ATPase activity was also decreased, though not significant, during hibernation. These results suggest that during hibernation, the bears are under increased oxidative stress, and have reduced activities of membrane-bound enzymes such as Ca(2+)/Mg(2+)-ATPase and Na(+)/K(+)-ATPase. These changes can be considered part of the adaptive for survival process of metabolic depression.

Animals↗
PubMed2002

Changes during hibernation in different phospholipid and free and esterified cholesterol serum levels in black bears.

During hibernation, fat is known to be the preferred source of energy. A detailed analysis of different phospholipids, as well as free and esterified cholesterol, was conducted to investigate lipid abnormalities during hibernation. The levels of total phospholipids and total cholesterol in the serum of black bears were found to increase significantly in hibernation as compared with the active state. Both free and esterified cholesterol were increased in the hibernating state in comparison with the active state (P < 0.05). The percentage increase during hibernation was more in free cholesterol (57%) than in esterified cholesterol (27%). Analysis of subclasses of serum phospholipids showed that choline containing phospholipids, i.e., sphingomyelin (SPG) (14%) and phosphatidylcholine (PC) (76%), are the major phospholipids in the serum of bear. The minor phospholipids included 8% of phosphatidylserine (PS) + phosphatidylinositol (PI), while phosphatidylethanolamine (PE) was only 2% of the total phospholipids. A comparison of phospholipid subclasses showed that PC, PS + PI and SPG were significantly increased, while PE was significantly decreased (P < 0.05) in the hibernating state as compared with the active state in black bears. These results suggest that the catabolism of phospholipids and cholesterol is decreased during hibernation in black bears, leading to their increased levels in the hibernating state as compared with the active state. In summary, our results indicate that serum cholesterol and phospholipid fractions (except PE) are increased during hibernation in bears. It is proposed that the increase of these lipids may be due to the altered metabolism of lipoproteins that are responsible for the clearance of the lipids.

Animals↗
PubMed2000

Morphological study of the heart innervation of bats Myotis daubentoni and Eptesicus serotinus (Microchiroptera: Vespertilionidae) during hibernation.

The capability of bats to have heart rates fewer than 10 beats/min during hibernation and greater than 700 beats/min during flight surprises biologists and cardiologists. Cardioacceleration of hibernating bats is considered to be a function of their intracardiac nervous system. In the present study we investigated the morphology of the heart innervation of ten M. daubentoni and four E. serotinus bats during their natural hibernation in order to determine which intracardiac structures may be involved in cardioacceleration during their short-term (in av. 15-30 min) arousal from hibernation. The primary conclusions were as follows: (1) The innervation pattern of bats differs from many mammals in that bats have: (a) a subepicardiac nerve plexus which is vastly developed and contains a large number of intrinsic ganglia on both atria and ventricles, and (b) very small diameter axons within the unmyelinated nerve fibres, from 0.15 to 0.7 microm. (2) During hibernation an intercellular space of the sinoatrial node of M. daubentoni bats was in part filled with a cottony substance which can presumably be considered to be a temporary barrier between the conductive cardiomyocytes and nerve fibres. (3) In the hibernating bats, the acetylcholine vesicles were aggregated in the synaptic bulbs away from the presynaptic membrane. Possibly, the aggregation of the acetylcholine vesicles is capable of modifying cholinergic influences on the heart activity of hibernating bats. (4) The dense cores of catecholamine synaptic vesicles within, adrenergic axon terminals were seldomly observed in hibernating bats. Therefore, catecholamines probably do not play a crucial role in the cardioacceleration of hibernating bats.

Animals↗
PubMed1998

Stimulation of tyrosine phosphorylation of a brain protein by hibernation.

Mammalian hibernation is a state of natural tolerance to severely decreased brain blood flow. As protein tyrosine phosphorylation is believed to be involved in the development of resistance to potentially cell-damaging insults, we used immunoblotting for the phosphotyrosine moiety to analyze extracts from various tissues of hibernating and nonhibernating ground squirrels. A single, hibernation-specific phosphoprotein was detected in the brain, but not in any other tissue tested. This protein, designated pp98 to reflect its apparent molecular weight, is distributed throughout the brain, and is associated with the cellular membrane fraction. The presence of the protein is tightly linked to the hibernation state; it is not present in contemporaneously assayed animals that are exposed to the same cold temperature as the hibernators, is present for the duration of a hibernation bout (tested from 1 to 14 days), and disappears within 1 hour of arousal from hibernation. The close association of pp98 with the hibernation state, its presence in cellular membranes, and the known properties of membrane phosphotyrosine proteins suggest that it may transduce a signal for adaptation to the limited availability of oxygen and glucose and low cellular temperature that characterizes hibernation in the ground squirrel.

Animals↗
PubMed1998

Enhanced vasoconstrictor responses in renal and femoral arteries of the golden hamster during hibernation.

1. The present study assessed local regulation of vascular tone of euthermic (control), cold control and hibernating golden hamsters. Sympathetic neurotransmission in the renal artery, the long term effects of hibernation on perivascular nerve activity, and the responsiveness of femoral artery to a number of neurotransmitters and hormones with both constrictor and dilator actions during hibernation are described. 2. The contractile responses of the renal arterial rings to transmural nerve stimulation (80 V, 0.1 ms, 4-64 Hz, for 1 s) were negligible in controls, significantly increased at higher frequencies of stimulation in cold controls and markedly enhanced in the hibernating group at all frequencies tested. The contractile responses to exogenous noradrenaline (NA; 0.1-100 microM) were significantly increased in the renal arteries of hibernating hamsters compared with controls, but not compared with cold controls. Responses to exogenous ATP (1-3000 microM) and KCl (120 mM) were similar among all experimental groups. 3. The maximal contractile responses of femoral arterial rings to the sympathetic co-transmitter ATP and 5-hydroxytryptamine were increased by approximately 124% and 99%, respectively, in hibernating compared with cold control preparations without a change in the concentration of agonist that produces half-maximal response. However, the responses to NA were not altered during hibernation. 4. Vasoconstriction of femoral arterial rings in response to arginine vasopressin was significantly enhanced in both cold controls and hibernating groups, while vasoconstriction in response to endothelin-1 and KCl was unaltered. 5. The dilator responses of femoral arterial rings to acetylcholine, sodium nitroprusside and adenosine were not different among the groups. 6. It is suggested that the marked augmentation of sympathetic neurotransmission, selective supersensitivity of the vascular smooth muscle to sympathetic contractile agents and unaltered vasodilatory mechanisms may provide a means for maintenance of vascular tone and peripheral resistance during hibernation.

Adenosine Triphosphate↗
PubMed1987

Patterns of reproductive hormone secretion in hibernating Turkish hamsters.

Changes in gonadal state and in circulating reproductive hormones [follicle-stimulating hormone (FSH), prolactin (PRL), and testosterone] were studied for 30 wk in male Turkish hamsters (Mesocricetus brandti) induced to hibernate by exposure to a short-day, cold environment [10:14-h light-dark (LD) cycle, 6 +/- 1 degree C]. Similar measures were compared in hamsters maintained under short-day warm conditions (10:14-h LD, 21 +/- 2 degrees C). A decrease in testicular size and in hormone levels was observed after 9-12 wk of short-day exposure in all animals. After 24 wk, hormone levels rose again, accompanied by testicular recrudescence, in short-day warm hamsters and in hamsters that failed to hibernate in the cold. For animals that hibernated the temporal pattern of endocrine and gonadal changes differed only slightly in comparison. Testicular recrudescence of hibernators lagged approximately 3 wk behind that of short-day warm hamsters. Hormone levels were generally lower in hibernators sampled during bouts of torpor than during bouts of spontaneous arousal from torpor. A marked elevation of serum FSH was observed in aroused hibernators well before the end of the hibernation season (at 21 wk of short-day exposure). Mean testosterone and PRL values had increased by wk 27, after hibernation was terminated in the majority of animals. These results indicate that testosterone may not be essential for the termination of the hibernation season. The data also suggest that an endogenous timing mechanism, resistant to the decreased body temperature experienced during torpor, may function to trigger a resurgence of the neuroendocrine-gonadal axis at the end of the winter season.

Animals↗
PubMed2003

Bone formation is not impaired by hibernation (disuse) in black bears Ursus americanus.

Disuse by bed rest, limb immobilization or space flight causes rapid bone loss by arresting bone formation and accelerating bone resorption. This net bone loss increases the risk of fracture upon remobilization. Bone loss also occurs in hibernating ground squirrels, golden hamsters, and little brown bats by arresting bone formation and accelerating bone resorption. There is some histological evidence to suggest that black bears Ursus americanus do not lose bone mass during hibernation (i.e. disuse). There is also evidence suggesting that muscle mass and strength are preserved in black bears during hibernation. The question of whether bears can prevent bone loss during hibernation has not been conclusively answered. The goal of the current study was to further assess bone metabolism in hibernating black bears. Using the same serum markers of bone remodeling used to evaluate human patients with osteoporosis, we assayed serum from five black bears, collected every 10 days over a 196-day period, for bone resorption and formation markers. Here we show that bone resorption remains elevated over the entire hibernation period compared to the pre-hibernation period, but osteoblastic bone formation is not impaired by hibernation and is rapidly accelerated during remobilization following hibernation.

Animals↗
PubMed1999

Gene expression in the brain across the hibernation cycle.

The purpose of this study was to characterize changes in gene expression in the brain of a seasonal hibernator, the golden-mantled ground squirrel, Spermophilus lateralis, during the hibernation season. Very little information is available on molecular changes that correlate with hibernation state, and what has been done focused mainly on seasonal changes in peripheral tissues. We produced over 4000 reverse transcription-PCR products from euthermic and hibernating brain and compared them using differential display. Twenty-nine of the most promising were examined by Northern analysis. Although some small differences were observed across hibernation states, none of the 29 had significant changes. However, a more direct approach, investigating expression of putative hibernation-responsive genes by Northern analysis, revealed an increase in expression of transcription factors c-fos, junB, and c-Jun, but not junD, commencing during late torpor and peaking during the arousal phase of individual hibernation bouts. In contrast, prostaglandin D2 synthase declined during late torpor and arousal but returned to a high level on return to euthermia. Other genes that have putative roles in mammalian sleep or specific brain functions, including somatostatin, enkephalin, growth-associated protein 43, glutamate acid decarboxylases 65/67, histidine decarboxylase, and a sleep-related transcript SD464 did not change significantly during individual hibernation bouts. We also observed no decline in total RNA or total mRNA during torpor; such a decline had been previously hypothesized. Therefore, it appears that the dramatic changes in body temperature and other physiological variables that accompany hibernation involve only modest reprogramming of gene expression or steady-state mRNA levels.

Animals↗
PubMed1992

[Effect of intraventricular injection of 6-hydroxydopamine on the initiation of hibernation in ground squirrels].

The effect of forced depletion of brain norepinephrine (NE) on the onset of hibernation was observed in the ground squirrel (Citellus dauricus) by intraventricular injection of 6-hydroxydopamine (6-OHDA). The results showed: (1) Intraventricular injection of 100-200 micrograms 6-OHDA, which depleted 50-60% NE, markedly facilitated the onset of hibernation, i.e. the average induction period for hibernation in the treated animals was significantly shorter than that of the natural hibernating animals. (2) The average total torpor time in the treated animals was longer than that of natural hibernating animals. (3) All hibernating animals treated with 6-OHDA were able to wake up from deep hibernation spontaneously and undergo normal hibernation bouts. The results indicate the decrease of NE system activity in brain is one important factor in triggering the onset of hibernation.

Animals↗
PubMed1992

Identification of novel blood proteins specific for mammalian hibernation.

Mammalian hibernation is a unique physiological adaptation that allows the sustainment of life under extremely low body temperatures. In the chipmunk, we found four proteins related specifically to hibernation. These proteins started to diminish in concentration in the blood before and disappeared during hibernation. These proteins reappeared in the blood as hibernation ceased and remained during nonhibernation. The complete or partial amino acid sequences of the four proteins showed that three (27-, 25-, and 20-kDa) were previously unknown, whereas another (55-kDa) is highly homologous with alpha 1-antitrypsin. The three novel proteins are homologous, indicating that they are a family. In the NH2-terminal regions of these proteins, a collagen-like amino acid sequence is present, whereas in their COOH-terminal regions, two sequences, Ser-Ala-Phe-Ala-Val-Lys and Val-Trp-Leu-Glu, are conserved. Analysis by sodium dodecyl sulfate-polyacrylamide gel electrophoresis under nonreducing conditions and gel permeation chromatography under denaturating conditions revealed that the four proteins form a 140-kDa complex in the plasma fraction. The novel proteins were detected in blood of another hibernator, the ground squirrel, but not in rodent nonhibernators, namely tree squirrels and rats. The present finding is the first identification of a hibernation-specific protein. The presence of specific proteins in hibernators suggests the involvement of genetic factors in the control of hibernation. These proteins provide valuable tools for understanding molecular mechanisms of mammalian hibernation.

Amino Acid Sequence↗
PubMed1992

Hibernating myocardium in patients with coronary artery disease: identification and clinical importance.

The term hibernating myocardium describes a particular outcome of myocardial ischemia in which myocytes show a chronically depressed contractile ability but remain viable. Revascularization of hibernating tissue causes a recovery of mechanical function that correlates with long-term survival. Therefore it is important clinically to distinguish hibernating from infarcted myocardium, since asynergies due to hibernation will improve on reperfusion, whilst those due to infarct will not. One suggested technique to identify hibernating myocardium is to stimulate the myocytes acutely, but briefly, by administration of inotropic agents while monitoring contractile function by echocardiography. We report our experience on the use of low dosages of dobutamine. Myocardial viability was validated by measuring the recovery in contraction of the akinetic areas after coronary artery bypass surgery by means of intraoperative epicardial echocardiography. The test has a sensitivity of 93% and a specificity of 78%. It is useful for identification of viable myocardium and also for quantification of intraoperative risk in individual patients. Limitations of this test are related to the presence of downregulation of beta receptors and to the impossibility of differentiating hibernating from stunned myocardium. Another useful technique of identifying hibernating myocardium is the use of radionuclear markers for viability. In our experience the two most important tests are (1) rest-redistribution imaging of thallium 201 (which has a high sensitivity of 93% but a low specificity of 44%) and (2) 99mTc-Sestamibi imaging, which provides information on both perfusion and function with a single injection. This latter technique allows differentiation between stunning and hibernating on the basis of coronary flow which is preserved in stunning and reduced in hibernation.

Cell Survival↗