Lipidomics Reveals Seasonal Shifts in a Large-Bodied Hibernator, the Brown Bear

Giroud, Sylvain; Chery, Isabelle; Bertile, Fabrice; Bertrand‐Michel, Justine; Tascher, Georg; Gauquelin‐Koch, Guillemette; Arnemo, Jon M.; Swenson, Jon E.; Singh, Navinder J.; Lefai, Étienne; Evans, Alina L.; Simon, Chantal; Blanc, Stéphane

doi:10.3389/fphys.2019.00389

Cited by 37 publications

(34 citation statements)

References 76 publications

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“…Accordingly, we found that the concentration of total fatty acids was elevated in the serum of hibernating bears, a finding in line with previous studies [5,30]. Considering both the amount and relative proportions of circulating lipids, our results are consistent with changes in serum lipid profiles during hibernation that have been previously published [5,9,10], notably an enrichment in DHA (22:6n-3) and depletions in ALA (18:3n-3) and EPA (20:5n-3), during winter compared to summer. Concomitantly, we observed a drop in arachidonic acid (AA) proportion, thus leading to a sharp increase in the DHA/AA ratio.…”

Section: Discussionsupporting

confidence: 93%

“…Brown bears (Ursus arctos) exhibit unique features, as they hibernate at mild hypothermia (32-35°C) and stay inside their dens for up to 7 months, without drinking, eating, defecating or urinating, and with no arousal episodes [3][4][5][6]. While denning, they reduce their metabolic rate by about 75% [7], and rely on mobilization of fat stores, which is reflected in increased circulating fatty acid concentration during winter [8][9][10].…”

Section: Introductionmentioning

confidence: 99%

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Specific shifts in the endocannabinoid system in hibernating brown bears

Boyer

Cussonneau

Brun

et al. 2020

Preprint

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In small hibernators, global downregulation of the endocannabinoid system (ECS), which is involved in modulating neuronal signaling, feeding behavior, energy metabolism, and circannual rhythms, has been reported to possibly drive physiological adaptation to the hibernating state. We hypothesized that specific changes should occur in hibernating brown bears ( Ursus arctos ) due to specific features, including hibernation during half the year at only mild hypothermia while remaining physically inactive without drinking or eating, and the absence of arousal episodes although bears remain sensitive to external disturbances. We explored circulating lipids and the ECS in plasma and metabolically active tissues (muscle and adipose tissue), in free-ranging subadult Scandinavian brown bears when both active and hibernating. In winter bear serum, in addition to a 2-fold increase in total fatty acid concentration, we found significant changes in relative proportions of circulating fatty acids, such as a 2-fold increase in docosahexaenoic acid and a decrease in arachidonic acid. In adipose and muscle tissues of hibernating bears, we found lower concentrations of both two major ligands for endocannabinoid receptors, 2-arachidonoylglycerol (2-AG) and anandamide (AEA). Gene expression was reduced for enzymes that synthesize endocannabinoid compounds, whereas an increase was observed for catabolic enzymes. Reduction in ECS tone may promote mobilization of fat stores and favor carbohydrate metabolism in skeletal muscle of hibernating bears. Additionally, high circulating of the endocannabinoid-like compound N-oleoylethanolamide (OEA) in winter could favor lipolysis and fatty acid oxidation in peripheral tissues. We also speculated on a role of OEA in the maintenance of torpor (reduction in locomotion), while promoting the capacity of bears to sense stimuli from the environment.

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Section: Discussionsupporting

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Specific shifts in the endocannabinoid system in hibernating brown bears

Boyer

Cussonneau

Brun

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Accordingly, we found that the concentration of total circulating fatty acids was elevated in hibernating bears, a nding in line with previous studies [5,44]. Considering both the amount and relative proportions of circulating lipids, our results are consistent with changes in serum and plasma lipid pro les during hibernation that have been previously published [5,9,10], notably an enrichment in DHA C22:6 n-3 and depletions in ALA C18:3 n-3 and EPA C20:5 n-3, during winter compared to summer. Whether the depletion in the ALA and EPA precursor species could be directly linked to the observed DHA increase remains to be elucidated.…”

Section: Discussionsupporting

confidence: 93%

“…Brown bears (Ursus arctos) exhibit unique features, as they hibernate at mild hypothermia (32-35°C) and can stay inside their dens for up to 7 months, without drinking, eating, defecating or urinating, and with no arousal episodes [3][4][5][6]. While denning, they reduce their metabolic rate by about 75% [7], and rely primarily on mobilization of fat stores, which is re ected by increased circulating fatty acid concentration and body fat store depletion during winter [8][9][10].…”

Section: Introductionmentioning

confidence: 99%

Specific shifts in the endocannabinoid system in hibernating brown bears

Boyer

Cussonneau

Brun

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

In small hibernators, global downregulation of the endocannabinoid system (ECS), which is involved in modulating neuronal signaling, feeding behavior, energy metabolism, and circannual rhythms, has been reported to possibly drive physiological adaptation to the hibernating state. In hibernating brown bears ( Ursus arctos ), we hypothesized that beyond an overall suppression of the ECS, seasonal shift in endocannabinoids compounds could be linked to bear’s peculiar features that include hibernation without arousal episodes and capacity to react to external disturbance. We explored circulating lipids in serum and the ECS in plasma and metabolically active tissues in free-ranging subadult Scandinavian brown bears when both active and hibernating. In winter bear serum, in addition to a 2-fold increase in total fatty acid concentration, we found significant changes in relative proportions of circulating fatty acids, such as a 2-fold increase in docosahexaenoic acid C22:6 n-3 and a decrease in arachidonic acid C20:4 n-6. In adipose and muscle tissues of hibernating bears, we found significant lower concentrations of 2-arachidonoylglycerol (2-AG), a major ligand of cannabinoid receptors 1 (CB1) and 2 (CB2). Lower mRNA level for genes encoding CB1 and CB2 were also found in winter muscle and adipose tissue, respectively. The observed reduction in ECS tone may promote fatty acid mobilization from body fat stores, and favor carbohydrate metabolism in skeletal muscle of hibernating bears. Additionally, high circulating level of the endocannabinoid-like compound N-oleoylethanolamide (OEA) in winter could favor lipolysis and fatty acid oxidation in peripheral tissues. We also speculated on a role of OEA in the conservation of an anorexigenic signal and in the maintenance of torpor during hibernation, while sustaining the capacity of bears to sense stimuli from the environment.

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“…High concentrations of phospholipids and cholesterol may be due to the shrinking of the membrane of the adipocytes caused by dehydration (Welinder et al, 2016). The high concentrations of free fatty acids (FA) and glycerol might be the result of their release from adipose tissue during hibernation (Welinder et al, 2016), with short chain (easier oxidation) of FAs being released and retained in muscle and tissue adipose than long FA chains, as it occurs in other hibernating mammals (Giroud et al, 2019). Long chain of FAs, such as Omega 3 and Omega 6, some of which are responsible for carbohydrate metabolism and protein sparing in bear muscles (Chazarin, Storey, et al, 2019), vary their concentration in muscles and plasma differently between the active and hibernating states (Giroud et al, 2018).…”

Section: Lipid Metabolismmentioning

confidence: 99%

Denning in brown bears

González-Bernardo

Russo

Valderrábano

et al. 2020

Ecology and Evolution

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Hibernation represents an adaptation for coping with unfavorable environmental conditions. For brown bears Ursus arctos, hibernation is a critical period as pronounced temporal reductions in several physiological functions occur. Here, we review the three main aspects of brown bear denning: (1) den chronology, (2) den characteristics, and (3) hibernation physiology in order to identify (a) proximate and ultimate factors of hibernation as well as (b) research gaps and conservation priorities. Den chronology, which varies by sex and reproductive status, depends on environmental factors, such as snow, temperature, food availability, and den altitude. Significant variation in hibernation across latitudes occurs for both den entry and exit. The choice of a den and its surroundings may affect individual fitness, for example, loss of offspring and excessive energy consumption. Den selection is the result of broad‐ and fine‐scale habitat selection, mainly linked to den insulation, remoteness, and availability of food in the surroundings of the den location. Hibernation is a metabolic challenge for the brown bears, in which a series of physiological adaptations in tissues and organs enable survival under nutritional deprivation, maintain high levels of lipids, preserve muscle, and bone and prevent cardiovascular pathologies such as atherosclerosis. It is important to understand: (a) proximate and ultimate factors in denning behavior and the difference between actual drivers of hibernation (i.e., factors to which bears directly respond) and their correlates; (b) how changes in climatic factors might affect the ability of bears to face global climate change and the human‐mediated changes in food availability; (c) hyperphagia (period in which brown bears accumulate fat reserves), predenning and denning periods, including for those populations in which bears do not hibernate every year; and (d) how to approach the study of bear denning merging insights from different perspectives, that is, physiology, ecology, and behavior.

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Lipidomics Reveals Seasonal Shifts in a Large-Bodied Hibernator, the Brown Bear

Cited by 37 publications

References 76 publications

Specific shifts in the endocannabinoid system in hibernating brown bears

Specific shifts in the endocannabinoid system in hibernating brown bears

Specific shifts in the endocannabinoid system in hibernating brown bears

Denning in brown bears

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