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PubMed1994

Thermal effects on neuronal activity in suprachiasmatic nuclei of hibernators and nonhibernators.

The temperature sensitivity of neuronal firing rates in the suprachiasmatic nuclei (SCN) of the hypothalami of rats and ground squirrels was studied in vitro. SCN from euthermic squirrels were studied during the hibernation season (winter) and during the summer. SCN from hibernating squirrels were also studied. Most properties of SCN cells from hibernators and nonhibernators were similar. Warm- and cold-sensitive neurons were observed in all groups, but cold-sensitive neurons were more common in SCN from hibernating squirrels. No evidence for temperature compensation of firing rate was accumulated; no cell was observed to fire below 16.6 degrees C. If the persistence of circadian rhythmicity is a function of action potential-dependent neurotransmission from the SCN, these results suggest that deep hibernation (5-17 degrees C) should be characterized by an absence of circadian fluctuation in temperature. Two possible adaptations for the shallow torpor seen at somewhat higher temperatures were observed in the SCN: 1) a relatively large population of cold-sensitive neurons and 2) a population of neurons with very high activation energies. Activation energy analysis suggested that most of the temperature-sensitive properties of these cells could be explained in terms of the thermal sensitivity of the sodium channel.

Action Potentials↗
PubMed1995

Rates of glucose utilization in brain of active and hibernating ground squirrels.

Rates of glucose utilization (CMRGlc) were determined in some cerebral structures of active warm- and cold-adapted ground squirrels and hibernating ground squirrels with [14C]deoxyglucose (DG) by direct chemical measurement of precursor and products in samples dissected from funnel-frozen brain. The rate of supply relative to demand of glucose and [14C]DG in brain of hibernating animals was similar to or greater than that of controls. [14C]DG cleared from the plasma in hibernators much more slowly than in active animals, and the level of unmetabolized [14C]DG in brain and the integrated specific activity of the precursor pool in plasma exceeded those of the active animals by 4- to 10-fold. At 45 min after an intravenous pulse of [14C]DG, the unmetabolized [14C]DG remaining in the brains of the hibernators accounted for approximately 96% of the total 14C compared with approximately 10-15% in the active animals. The value of lambda, a factor contained in the lumped constant of the operational equation of the [14C]DG method, was estimated for each animal and found to be relatively constant over the sixfold range of glucose levels in the brains of all animals. Calculated CMRGlc in squirrels in deep hibernation was only 1-2% of the values in active animals.

Animals↗
PubMed1997

Effects of plasma from hibernating ground squirrels on monocyte-endothelial cell adhesive interactions.

Adhesion and subsequent penetration of leukocytes into central nervous system ischemic tissue proceeds via a coordinated inflammatory mechanism involving adhesion molecules at the blood-endothelium interface. Mammalian hibernation is a state of natural tolerance to severely reduced blood flow-oxygen delivery (i.e., ischemia). Hibernating thirteen-lined ground squirrels were investigated in an attempt to identify factors responsible for regulating this tolerance. Since leukocytopenia is closely associated with entrance into hibernation, the role of leukocyte adhesion to endothelium in this phenomenon was examined. Intercellular adhesion molecule-1 (ICAM-1) is expressed by endothelium and regulates interactions with circulating leukocytes that may result in margination or extravasation. ICAM-1 expression by rat cerebral microvascular endothelial cells (EC) cultured with plasma from hibernating (HP) or nonhibernating (NHP) thirteen-lined ground squirrels was dose dependently increased by HP and, to a lesser extent, by NHP. Treatment of EC with HP coincidentally induced significantly greater increases in monocyte adhesion to EC (37.2%) than were observed with NHP (23.9%). Study of the effects of HP and NHP on monocyte adhesion to EC may identify mechanisms responsible for ischemic tolerance in hibernators and could lead to the development of novel therapeutic approaches to the treatment of stroke.

Animals↗
PubMed1998

Differential regulation of uncoupling protein gene homologues in multiple tissues of hibernating ground squirrels.

Nonshivering thermogenesis in brown adipose tissue (BAT) provides heat through activation of a mitochondrial uncoupling protein (UCP1), which causes futile electron transport cycles without the production of ATP. Recent discovery of two molecular homologues, UCP2, expressed in multiple tissues, and UCP3, expressed in muscle, has resulted in investigation of their roles in thermoregulatory physiology and energy balance. To determine the expression pattern of Ucp homologues in hibernating mammals, we compared relative mRNA levels of Ucp1, -2, and -3 in BAT, white adipose tissue (WAT), and skeletal muscle of arctic ground squirrels (Spermophilus parryii) hibernating at different ambient and body temperatures, with levels determined in tissues from ground squirrels not in hibernation. Here we report significant increases in mRNA levels for Ucp2 in WAT (1. 6-fold) and Ucp3 in skeletal muscle (3-fold) during hibernation. These results indicate the potential for a role of UCP2 and UCP3 in thermal homeostasis during hibernation and indicate that parallel mechanisms and multiple tissues could be important for nonshivering thermoregulation in mammals.

Adipose Tissue↗
PubMed2000

Regulation of body temperature and energy requirements of hibernating alpine marmots (Marmota marmota).

Body temperature and metabolic rate were recorded continuously in two groups of marmots either exposed to seasonally decreasing ambient temperature (15 to 0 degrees C) over the entire hibernation season or to short-duration temperature changes during midwinter. Hibernation bouts were characterized by an initial 95% reduction of metabolic rate facilitating the drop in body temperature and by rhythmic fluctuations during continued hibernation. During midwinter, we observed a constant minimal metabolic rate of 13.6 ml O(2) x kg(-1) x h(-1) between 5 and 15 degrees C ambient temperature, although body temperature increased from 7.8 to 17.6 degrees C, and a proportional increase of metabolic rate below 5 degrees C ambient temperature. This apparent lack of a Q(10) effect shows that energy expenditure is actively downregulated and controlled at a minimum level despite changes in body temperature. However, thermal conductance stayed minimal (7.65 +/- 1.95 ml O(2) x kg(-1) x h(-1) x degrees C(-1)) at all temperatures, thus slowing down cooling velocity when entering hibernation. Basal metabolic rate of summer-active marmots was double that of winter-fasting marmots (370 vs. 190 ml O(2) x kg(-1) x h(-1)). In summary, we provide strong evidence that hibernation is not only a voluntary but a well-regulated strategy to counter food shortage and increased energy demands during winter.

Animals↗
PubMed2001

Expression of a chimeric retroviral-lipase mRNA confers enhanced lipolysis in a hibernating mammal.

Hibernating mammals can survive several months without feeding by limiting their carbohydrate catabolism and using triacylglycerols stored in white adipose tissue (WAT) as their primary source of fuel. Here we show that a lipolytic enzyme normally found in the gut, pancreatic triacylglycerol lipase (PTL), is expressed in WAT of hibernating 13-lined ground squirrels (Spermophilus tridecemlineatus). PTL expressed in WAT is encoded by an unusual chimeric retroviral-PTL mRNA approximately 500 bases longer than the predominant PTL message found in other ground squirrel tissues. Seasonal measurements detect the chimeric mRNA and PTL enzymatic activity in WAT before and during hibernation, with both showing their lowest observed levels 1 wk after hibernation concludes in mid-March. PTL is expressed in addition to hormone-sensitive lipase, the enzyme typically responsible for hydrolysis of triacylglycerols in WAT. Because of the distinct catalytic and regulatory properties of both enzymes, this dual-triacylglycerol lipase system provides a means by which the fuel requirements of hibernating 13-lined ground squirrels can be met without interruption.

Adipose Tissue↗
PubMed2002

Invited review: molecular adaptations in mammalian hibernators: unique adaptations or generalized responses?

Hibernators are unique among mammals in their ability to attain, withstand, and reverse low body temperatures. Hibernators repeatedly cycle between body temperatures near zero during torpor and 37 degrees C during euthermy. How do these mammals maintain cardiac function, cell integrity, blood fluidity, and energetic balance during their prolonged periods at low body temperature and avoid damage when they rewarm? Hibernation is often considered an example of a unique adaptation for low-temperature function in mammals. Although such adaptation is apparent at the level of whole animal physiology, it is surprisingly difficult to demonstrate clear examples of adaptations at the cellular and biochemical levels that improve function in the cold and are unique to hibernators. Instead of adaptation for improved function in the cold, the key molecular adaptations of hibernation may be to exploit the cold to depress most aspects of biochemical function and then rewarm without damage to restore optimal function of all systems. These capabilities are likely due to novel regulation of biochemical pathways shared by all mammals, including humans.

Adaptation, Physiological↗
PubMed2003

Pancreatic triacylglycerol lipase in a hibernating mammal. II. Cold-adapted function and differential expression.

Thirteen-lined ground squirrels (Spermophilus tridecemlineatus) exploit the low-temperature activity of pancreatic triacylglycerol lipase (PTL) during hibernation. Lipolytic activity at body temperatures associated with hibernation was examined using recombinant ground squirrel and human PTLs expressed in yeast. Both the human and ground squirrel enzymes displayed high activity at temperatures as low as 0 degrees C and showed Q10 values of 1.2-1.5 over a range of 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. Western blots show elevated levels of PTL protein during hibernation in both heart and white adipose tissue (WAT). Significant increases in PTL gene expression are seen in heart, WAT, and testes; but not in pancreas, where PTL mRNA levels are highest. Upregulation of PTL in testes is also accompanied by expression of the PTL-specific cofactor, colipase. The multi-tissue expression of PTL during hibernation supports its role as a key enzyme that shows high activity at low temperatures.

Adipose Tissue↗
PubMed1995

Parasympathetic influence on heart rate in euthermic and hibernating ground squirrels.

The relative role of the parasympathetic nervous system during deep hibernation is enigmatic. Conflicting hypotheses exist, and both sides draw support from investigations of vagal influence on the heart. Recent studies have shown cardiac chronotropic and inotropic effects of parasympathetic stimulation and inhibition in isolated hearts and anesthetized animals at hibernating body temperatures. No studies, however, have demonstrated such occurrences in undisturbed deeply hibernating animals. The present study documents respiratory-related alterations in heart rate during euthermia and hibernation at ambient temperatures of 15, 10 and 5 degrees C mediated by parasympathetic influence. During quiet wakefulness, euthermic squirrels breathed continuously and exhibited a 29% acceleration in heart rate during inspiration. During deep undisturbed hibernation, at 15, 10 and 5 degrees C ambient temperature, animals exhibited an episodic breathing pattern and body temperatures were slightly above ambient temperature. At each temperature, heart rate during the respiratory episode was greater than that during the apnea. The magnitude of this ventilatory tachycardia decreased with ambient temperature, being 108% at 15 degrees C, 32% at 10 degrees C and 11.5% at 5 degrees C. Animals exposed to 3% CO2 at 5 degrees C, which significantly increased ventilation, still exhibited an 11.7% increase in heart rate during breathing. Thus, the magnitude of the ventilation tachycardia was independent of the level of ventilation, at least over the range studied. Inhibition of vagus nerve conduction at 5 degrees C was achieved using localized nerve block. This led to an increase in apneic heart rate and abolished the ventilatory tachycardia.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗
PubMed2004

Delta opioid peptide (D-Ala 2, D-Leu 5) enkephalin: linking hibernation and neuroprotection.

Hibernation is a potential protective strategy for the peripheral, as well as for the central nervous system. A protein factor termed hibernation induction trigger (HIT) was found to induce hibernation in summer-active ground squirrels. Purification of HIT yielded an 88-kD peptide that is enriched in winter hibernators. Partial sequence of the 88-kD protein indicates that it may be related to the inhibitor of metalloproteinase. Using opioid receptor antagonists to elucidate the mechanisms of HIT, it was found that HIT targeted the delta opioid receptors. Indeed, delta opioid (D-Ala 2, D-Leu 5) enkephalin (DADLE) was shown to induce hibernation. Specifically, HIT and DADLE were found to prolong survival of peripheral organs, such as the lung, the heart, liver, and kidney preserved en bloc or as a single preparation. In addition, DADLE has been recently demonstrated to promote survival of neurons in the central nervous system. Exposure to DADLE dose-dependently enhanced cell viability of cultured primary rat fetal dopaminergic cells. Subsequent transplantation of these DADLE-treated dopaminergic cells into the Parkinsonian rat brain resulted in a two-fold increase in surviving grafted cells. Interestingly, delivery of DADLE alone protected against dopaminergic depletion in a rodent model of Parkinson s disease. Similarly, DADLE blocked and reversed the dopaminergic terminal damage induced by methamphetamine (METH). Such neuroprotective effects of DADLE against METH neurotoxicity was accompanied by attenuation of mRNA expressions of a tumor necrosis factor p53 and an immediate early gene c-fos. In parallel to these beneficial effects of DADLE on the dopaminergic system, DADLE also ameliorated the neuronal damage induced by ischemia-reperfusion following a transient middle cerebral artery occlusion. In vitro replication of this ischemia cell death by serum-deprivation of PC12 cells revealed that DADLE exerted neuroprotection in a naltrexone-sensitive manner. These results taken together suggest that DADLE stands as a novel therapeutic agent. In this review paper, we present laboratory evidence supporting the use of DADLE for protection of peripheral and central nervous system.

Animals↗
PubMedDate not supplied

[The state-dependent action of neuropeptides and monoamines on the background neuronal activity of the medial septal area in hibernating animals].

Neuronal activity of the medial septal area (MS-DB) was recorded extracellularly in brain slices from two groups of Yakutian ground squirrels Citellus undulatus--hibernating (winter period) and actively waking (summer period). Effects of three neuropeptides identified in the brain of hibernators (TSKYR, TSKY, and DY) and of two monoamines (serotonin and noradrenaline) on spontaneous activity were analyzed. All neuropeptides reversibly changed the levels of the background activity, but in the hibernating ground squirrels (HGS) the level of reactivity (47-56%) was significantly higher than in the waking ground squirrels (WGS, 25-30%). Serotonin also showed some tendency to higher efficacy in the HGS. Only noradrenaline was equally effective and had absolutely dominating excitatory effect in both states, although the level of excitation in the HGS was higher. All other substances evoked excitatory and inhibitory effects in various proportions. Their distribution was state-dependent, the rate of development, intensity and duration of the effects were greater in the HGS. The experiments confirmed the data on higher excitability and reactivity of the septal neurons in the state of hibernation. It is suggested that the tested neuropeptides may participate in the control of hibernation.

Animals↗
PubMedDate not supplied

[Effects of sleep on ovary development during hibernation and aestivation in the dormouse (Eliomys quercinus L.)(author's transl)].

Hibernation does not correspond to a period of rest of the ovary, nor to the prolongation of a period of anoestrus. Hibernation is necessary for the normal course of the period of genital activity. Its suppression tends to modify more or less severely the physiological equilibrium implicated in the control of genital activities. However, the animal can find a more or less normal rythm even if is deprived of hibernation during the course of a second year. Prolongation of hibernation in hemicastrated animals during the entire period of genital activity suppresses the ovular discharge and the ovulating secretion of FSH and LH, without affecting the tonic secretions of FSH. It inhibits the phenomenon of compensatory hypertrophy. However, in hemicastrated animals deprived of hibernation, the reaction to hemicastration does not take place nor during anoestrus nor during mid-december or mid-march but only when the period of genital activity begins again.

Anestrus↗
PubMedDate not supplied

Fine structure and photoperiodical seasonal changes in Pars tuberalis of hibernating bats.

In Pars tuberalis (PT) of pituitary gland of hibernating bats, extending cranially along the ventral face of the hypothalamic median eminence, around the hypophyseal stalk, and caudally continuing in the Pars distalis (PD), pt specific cells, follicular cells and gonadotropic cells were distinguished. Pt specific cells contain peculiar secretory granules positive to lectin WGA and negative to lectins LFA and PNA, positive to S-100 protein labeling and to PD hormones antisera. During hibernation they present a low numerical density of both secretory granules and melatonin binding sites. After light exposure, on the other hand, the latter increase in density and are associated with marked secretion synthetic activity and exocytosis. These aspects result to be more balanced in animals sacrificed during summer. These changes seem to support the hypothesis of marked annual changes even in animal species with seasonal rhythmicity of metabolisms and gonads. Follicular cells, organized in closed follicles, have slightly developed RER and Golgi apparatus during hibernation, whereas they seem to show an increased secretory activity after light exposure and during summer. In perinuclear and supranuclear cytoplasm, glycogen particles clusters (peculiar of hibernation), cilia 9+2 and multivesicular bodies were identified. Concerning FSH cells, a reduced numerical density during hibernation, the secretory granules morphological characteristics and their probable involvement in photoperiod-linked reproductive functions are investigated.

Animals↗
PubMedDate not supplied

[The behavior of titin and the proteins of its family from skeletal muscles of ground squirrel (Citellus undulatus) during hibernation and rats under conditions of simulated microgravity].

By the use of SDS PAGE, the behavior of titin and MyBP-C in fast (m. psoas) as well as titin and MyBP-X in slow (m. soleus) muscles of ground squirrels (Citellus undulatus) during hibernation was compared with the behavior of titin and MyBP-X in rat m. soleus under conditions of simulated microgravity. A decrease in the amount of titin 1 and MyBP-C relative to that of myosin heavy chains by approximately 30% and approximately 40%, correspondingly, in muscles of hibernating and arousing ground squirrels was revealed in comparison with active animals. No differences in the relative amount of MyBP-X in m. soleus of hibernating, arousing and active ground squirrels were found. Under conditions of simulated microgravity, a decrease in the amount of titin 1 by approximately 2 times and MyBP-X by approximately1.5 times relative to that of myosin heavy chains in rat m. soleus was observed. By the method of SDS PAGE modified by us, an almost twofold decrease in the amount of short isovariants of the titin N2A isoform relative to that of myosin heavy chains was shown in muscles of hibernating and arousing ground squirrels, whereas no changes were found in the amount of long titin isovariants. The conditions of simulated microgravity resulted in a twofold decrease in the relative amount of both short and long titin isovariants in rat m. soleus. The results indicate that hibernating ground squirrels have an evolutionarily determined adaptive mechanism of selective degradation of fast muscle fibers and preservation or increase of slow fibers, as the most economic and energetically advantageous, with proteins typical of them. The microgravitation of nonhibernating animals (rats) leads to a non-selective degradation of MyBP-X and titin isovariants, which contributes to considerable atrophy of soleus fibers.

Adaptation, Physiological↗
PubMedDate not supplied

[Myosin light chains of skeletal and cardiac muscles of ground squirrel Citillus undulatus in different periods of hibernation].

The isoform composition of myosin light chains and the extent of their phosphorylation in skeletal and cardiac muscles of ground squirrel Citellus undulatus in different periods of hibernation were studied. Regulatory myosin light chains of skeletal muscles of hibernating ground squirrels were completely dephosphorylated, while 25% of these light chains in active animals were phosphorylated. During hibernation, a shift of isoform composition of essential and regulatory skeletal muscle myosin light chains toward slower isoforms was observed, which is evidenced by the data obtained on m. psoas and on the totality of all skeletal muscles. In the atrial myocardium of hibernating ground squirrels, ventricular myosin light chains 1 (up to 60%) were registered. In contrast, during arousal of ground squirrels, in ventricular myocardium the appearance of atrial myosin light chains 1 (up to 30%) was revealed. A possible role of posttranslation changes in myosin light chains and their isoform shifts in the hibernation scenario is discussed.

Animals↗
PubMedDate not supplied

[Seasonal changes in phosphorylation of myosin regulatory light chains and C-protein in myocardium of hibernating ground squirrel Citellus undulatus].

A comparative study concerning the extent of phosphorylation of myosin regulatory light chains and C-protein from the left ventricle of hibernating ground squirrel Citellus undulatus during the periods of hibernation and activity was carried out. During hibernation, regulatory light chains of ground squirrel were found to be completely dephosphorylated. In active animals, the share of phosphorylated light chains averages 40-45% of their total amount. The extent of phosphorylation of the cardiac C-protein during hibernation is about two times higher than that in the active state. Seasonal differences in phosphorylation of the two proteins of ground squirrel myocardium are discussed in the context of adaptation to hibernation.

Animals↗
PubMedDate not supplied

[The inhibition of succinate, beta-oxybutyrate and glutamate transport in the liver mitochondria of hibernating susliks].

Studies have been made on the permeability of the inner membrane of the liver mitochondria from hibernating and active ground squirrels for succinate, glutamate, hydroxybutyrate and inorganic phosphate. The permeability was calculated from the rate of mitochondrial swelling in 100 mM ammonium salts of the substrates and phosphate. It was shown that the rate of mitochondrial swelling in hibernating animals is 2--3 times lower than in active ones, being essentially identical in a solution of ammonium phosphate. It was concluded that the permeability of the inner mitochondrial membrane for the substrates decreases in hibernating animals, remaining unaffected for phosphate. Calcium-induced activation of membrane phospholipase A2 facilitates the transport of oxidative substrates into the mitochondria of hibernating ground squirrels, significant increase in the mitochondrial respiration being simultaneously observed. The data obtained suggest that inhibition of transport of oxidative substrates is one of the main factors which account for a low respiration rate in the mitochondria of hibernating animals.

3-Hydroxybutyric Acid↗
PubMedDate not supplied

[The intensity of oxidative phosphorylation and the function of the adenylate system in the liver mitochondria of active and hibernating susliks Citellus undulatus].

The state of adenylate system and intensity of oxidative phosphorylation in liver mitochondria of active and hibernating ground squirrels were studied depending on the concentration of extramitochondrial Ca2+ ([Ca2+]ex). It was shown that at [Ca2+]ex.10(-7) M, the content of ATP as well as ATP/ADP ratio are slightly lower in the mitochondria of hibernating ground squirrels than in the mitochondria of active animals. The other parameters of the adenylate system under the same conditions differ insignificantly. [Ca2+]ex increase to 10(-6) M has little effect on the parameters of the adenylate system of active animals. On the contrary, the mitochondria of hibernating ground squirrels are strongly affected: the level of ATP is 1.5-fold and the ratio of ATP/ADP is almost 2-fold decreased. At both [Ca2+]ex the intensity of oxidative phosphorylation is essentially higher in the mitochondria of active ground squirrels. With increasing [Ca2+]ex the rate of ATP synthesis decreases, and in the mitochondria of hibernating animals the decrease is more pronounced than in the mitochondria of active animals. Thus, oxidative phosphorylation and adenylate system of mitochondria from hibernating ground squirrels are more sensitive to [Ca2+]ex increase than those of the mitochondria of active animals.

Adenosine Diphosphate↗