Abstract
Polyunsaturated fatty acids (PUFAs) exert several important functions across organ systems. During winter, hibernators divert PUFAs from oxidation, retaining them in their tissues and membranes, to ensure proper body functions at low body temperature. PUFAs are also precursors of eicosanoids with pro- and anti-inflammatory properties. This study investigated seasonal changes in eicosanoid metabolism of free-ranging brown bears (Ursus arctos). By using a lipidomic approach, we assessed (1) levels of specific omega-3 and omega-6 fatty acids involved in the eicosanoid cascade and (2) concentrations of eicosanoids in skeletal muscle and blood plasma of winter hibernating and summer active bears. We observed significant seasonal changes in the specific omega-3 and omega-6 precursors. We also found significant seasonal alterations of eicosanoid levels in both tissues. Concentrations of pro-inflammatory eicosanoids, such as thromboxane B2, 5-hydroxyeicosatetraenoic acid (HETE), and 15-HETE and 18-HETE, were significantly lower in muscle and/or plasma of hibernating bears compared to summer-active animals. Further, plasma and muscle levels of 5,6-epoxyeicosatrienoic acid (EET), as well as muscle concentration of 8,9-EET, tended to be lower in bears during winter hibernation vs. summer. We also found lower plasma levels of anti-inflammatory eicosanoids, such as 15dPGJ2 and PGE3, in bears during winter hibernation. Despite of the limited changes in omega-3 and omega-6 precursors, plasma and muscle concentrations of the products of all pathways decreased significantly, or remained unchanged, independent of their pro- or anti-inflammatory properties. These findings suggest that hibernation in bears is associated with a depressed state of the eicosanoid cascade.
Highlights
To meet energy demands during winter, hibernators rely on body fat stores that they have accumulated during the previous summer (Geiser and Kenagy 1993)
Deer mice (Peromyscus maniculatus) have been found to increase the amount of omega-6 polyunsaturated fatty acids (PUFAs) in leg muscle when exposed to short photoperiod (Geiser et al 2007), and alpine marmots (Marmota marmota) transfer omega-6 PUFAs from white adipose tissue (WAT) to heart and liver phospholipids (PLs) at a high rate shortly before hibernation (Arnold et al 2011)
Levels of 5-hydroxyeicosatetraenoic acid (HETE), 8-HETE, and 15-HETE were significantly lower in muscle tissues of bears in winter hibernation than during the summer active period (Fig. 4)
Summary
To meet energy demands during winter, hibernators rely on body fat stores that they have accumulated during the previous summer (Geiser and Kenagy 1993). Deer mice (Peromyscus maniculatus) have been found to increase the amount of omega-6 PUFAs in leg muscle when exposed to short photoperiod (Geiser et al 2007), and alpine marmots (Marmota marmota) transfer omega-6 PUFAs from WAT to heart and liver phospholipids (PLs) at a high rate shortly before hibernation (Arnold et al 2011) In hibernators, these changes in lipid composition are expected to ensure proper body functions at low Tb during torpor, possibly through the maintenance of lipid fluidity (Aloia and Raison 1989; Sinensky 1974; Tiku et al 1996) and/or the regulation of membrane proteins by specific lipids (see Arnold et al 2015 for review; Giroud et al 2013; Ruf and Arnold 2008)
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