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Low body temperature governs the decline of circulating lymphocytes during hibernation through sphingosine-1-phosphate.

ABSTRACT: Hibernation is an energy-conserving behavior consisting of periods of inhibited metabolism ('torpor') with lowered body temperature. Torpor bouts are interspersed by arousal periods, in which metabolism increases and body temperature returns to euthermia. In deep torpor, the body temperature typically decreases to 2-10 °C, and major physiological and immunological changes occur. One of these alterations constitutes an almost complete depletion of circulating lymphocytes that is reversed rapidly upon arousal. Here we show that torpor induces the storage of lymphocytes in secondary lymphoid organs in response to a temperature-dependent drop in plasma levels of sphingosine-1-phosphate (S1P). Regulation of lymphocyte numbers was mediated through the type 1 S1P receptor (S1P(1)), because administration of a specific antagonist (W146) during torpor (in a Syrian hamster at ?8 °C) precluded restoration of lymphocyte numbers upon subsequent arousal. Furthermore, S1P release from erythrocytes via ATP-binding cassette (ABC)-transporters was significantly inhibited at low body temperature (4 °C) but was restored upon rewarming. Reversible lymphopenia also was observed during daily torpor (in a Djungarian hamster at ± 25 °C), during forced hypothermia in anesthetized (summer-active) hamsters (at ± 9 °C), and in a nonhibernator (rat at ?19 °C). Our results demonstrate that lymphopenia during hibernation in small mammals is driven by body temperature, via altered plasma S1P levels. S1P is recognized as an important bioactive lipid involved in regulating several other physiological processes as well and may be an important factor regulating additional physiological processes in hibernation as well as in mediating the effects of therapeutic hypothermia in patients.

SUBMITTER: Bouma HR

PROVIDER: S-EPMC3033260 | biostudies-literature | 2011 Feb

REPOSITORIES: biostudies-literature

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Low body temperature governs the decline of circulating lymphocytes during hibernation through sphingosine-1-phosphate.

Bouma Hjalmar R HR Kroese Frans G M FG Kok Jan Willem JW Talaei Fatimeh F Boerema Ate S AS Herwig Annika A Draghiciu Oana O van Buiten Azuwerus A Epema Anne H AH van Dam Annie A Strijkstra Arjen M AM Henning Robert H RH

Proceedings of the National Academy of Sciences of the United States of America 20110118 5

Hibernation is an energy-conserving behavior consisting of periods of inhibited metabolism ('torpor') with lowered body temperature. Torpor bouts are interspersed by arousal periods, in which metabolism increases and body temperature returns to euthermia. In deep torpor, the body temperature typically decreases to 2-10 °C, and major physiological and immunological changes occur. One of these alterations constitutes an almost complete depletion of circulating lymphocytes that is reversed rapidly ...[more]

PMID: 21245336

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Project description:Hibernation has been selected for increasing survival in harsh climatic environments. Seasonal variability in temperature may push the body temperatures of hibernating animals across boundaries of alternative states between euthermic temperature and torpor temperature, typical of either hibernation or summer dormancy. Nowadays, wearable electronics present a promising avenue to assess the occurrence of criticality in physiological systems, such as body temperature fluctuating between attractors of activity and hibernation. For this purpose, we deployed temperature loggers on two hibernating edible dormice for an entire year and under Mediterranean climate conditions. Highly stochastic body temperatures with sudden switches over time allowed us to assess the reliability of statistical leading indicators to anticipate tipping points when approaching a critical transition. Hibernation dynamics showed flickering, a phenomenon occurring when a system rapidly moves back and forth between two alternative attractors preceding the upcoming major regime shift. Flickering of body temperature increased when the system approached bifurcations, which were also anticipated by several metric- and model-based statistical indicators. Nevertheless, some indicators did not show a pattern in their response, which suggests that their performance varies with the dynamics of the biological system studied. Gradual changes in air temperature drove transient between states of hibernation and activity, and also drove hysteresis. For hibernating animals, hysteresis may increase resilience when ending hibernation earlier than the optimal time, which may occur in regions where temperatures are sharply rising, especially during winter. Temporal changes in early indicators of critical transitions in hibernation dynamics may help to understand the effects of climate on evolutionary life histories and the plasticity of hibernating organisms to cope with shortened hibernation due to global warming.

Project description:BackgroundDespite centuries of research, debate remains on the scaling of metabolic rate to mass especially for intraspecific cases. The high variation of body mass within brown bears presents a unique opportunity to study the intraspecific effects of body mass on physiological variables. The amplitude of metabolic rate reduction in hibernators is dependent on body mass of the species. Small hibernators have high metabolic rates when euthermic but experience a drastic decrease in body temperature during torpor, which is necessary to reach a very low metabolic rate. Conversely, large hibernators, such as the brown bear (Ursus arctos), show a moderate decrease in temperature during hibernation, thought to be related to the bear's large size. We studied body mass, abdominal body temperature, heart rate, and accelerometer-derived activity from 63 free-ranging brown bears (1-15 years old, 15-233 kg). We tested for relationships between body mass and body temperature, heart rate, and hibernation duration.ResultsThe smallest individuals maintained lower body temperatures during hibernation, hibernated longer, and ended hibernation later than large bears. Unlike body temperature, winter heart rates were not associated with body mass. In summer, the opposite pattern was found, with smaller individuals having higher body temperature and daytime heart rates. Body mass was associated with body temperature in the winter hypometabolic state, even in a large hibernating mammal. Smaller bears, which are known to have higher thermal conductance, reached lower body temperatures during hibernation. During summer, smaller bears had higher body temperatures and daytime heart rates, a phenomenon not previously documented within a single mammalian species.ConclusionWe conclude that the smallest bears hibernated more deeply and longer than large bears, likely from a combined effect of basic thermodynamics, the higher need for energy savings, and a lower cost of warming up a smaller body.

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Low body temperature governs the decline of circulating lymphocytes during hibernation through sphingosine-1-phosphate.

Publications

Low body temperature governs the decline of circulating lymphocytes during hibernation through sphingosine-1-phosphate.

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