Hormonal changes and energy substrate availability during the hibernation cycle of Syrian hamsters Mathieu Weitten a,b , Jean-Patrice Robin a,b , Hugues Oudart a,b , Paul Pévet c , Caroline Habold a,b, ⁎ a Université de Strasbourg, IPHC-DEPE, 23 rue Becquerel, 67087 Strasbourg, France b CNRS, UMR 7178, 23 rue Becquerel, 67087 Strasbourg, France c CNRS, Département de Neurobiologie des Rythmes, Institut des Neurosciences Cellulaires et Intégratives, UPR-3212, 5 rue Blaise Pascal, 67084 Strasbourg, France abstract article info Article history: Received 19 May 2013 Revised 23 August 2013 Accepted 24 August 2013 Available online 1 September 2013 Keywords: Mesocricetus auratus Torpor bout Periodic arousal Adipokines Incretins Food-storing behavior Animals have to adapt to seasonal variations in food resources and temperature. Hibernation is one of the most efficient means used by animals to cope with harsh winter conditions, wherein survival is achieved through a sig- nificant decrease in energy expenditure. The hibernation period is constituted by a succession of torpor bouts (hypometabolism and decrease in body temperature) and periodic arousals (eumetabolism and euthermia). Some species feed during these periodic arousals, and thus show different metabolic adaptations to fat-storing spe- cies that fast throughout the hibernation period. Our study aims to define these metabolic adaptations, including hormone (insulin, glucagon, leptin, adiponectin, GLP-1, GiP) and metabolite (glucose, free fatty acids, triglycerides, urea) profiles together with body composition adjustments. Syrian hamsters were exposed to varied photoperiod and temperature conditions mimicking different phases of the hibernation cycle: a long photoperiod at 20 °C (LP20 group), a short photoperiod at 20 °C (SP20 group), and a short photoperiod at 8 °C (SP8). SP8 animals were sampled either at the beginning of a torpor bout (Torpor group) or at the beginning of a periodic arousal (Arousal group). We show that fat store mobilization in hamsters during torpor bouts is associated with decreased circulat- ing levels of glucagon, insulin, leptin, and an increase in adiponectin. Refeeding during periodic arousals results in a decreased free fatty acid plasma concentration and an increase in glycemia and plasma incretin concentrations. Reduced incretin and increased adiponectin levels are therefore in accordance with the changes in nutrient avail- ability and feeding behavior observed during the hibernation cycle of Syrian hamsters. © 2013 Elsevier Inc. All rights reserved. Introduction Hibernation enables small mammals to cope with seasonal changes in food resources and allows them to limit energy expenditure for heat production in a cold environment. It is a succession of periods of hypometabolism associated with decreases in body temperature, called torpor bouts, and periodic arousals during which the animal returns to eumetabolism and euthermia (reviewed in: Heldmaier et al., 2004). Most species do not feed during hibernation and only rely on body reserves to fulfill energy requirements (fat-storing species), whereas other species hoard food in a burrow (food-storing species) and feed be- tween torpor bouts (reviewed in: Humphries et al., 2001; Geiser, 2004). In both cases, hibernation can be considered as a fasting state of variable duration (from 1 day in food-storing to several months in fat-storing species; Humphries et al., 2003). Many studies have focused on the use of energy substrates during different phases of the hibernation period. Measurements of the respi- ratory quotient (RQ) of an organism show that during torpor bouts, energy expenditure is almost exclusively provided by the oxidation of lipids (RQ close to 0.7) (Buck and Barnes, 2000; Kayser, 1952). During early periodic arousal (the warming-up phase), the increase in body temperature to 12–16 °C is accompanied by an increase of the RQ to 1.0, indicating the oxidation of carbohydrate (Heldmaier et al., 2004) and/or ventilation of CO 2 accumulated during torpor (Malan et al., 1988). Another approach to the study of energy substrate use during the hibernation cycle consists of measuring the activity of key enzymes involved in metabolic pathways, and more recently, the measurement of gene expressions during hibernation versus the active phase. These studies show that overall glucose utilization is reduced in favor of fat oxidation during torpor bouts (reviewed in: Dark, 2005). This shift of energy metabolism is accompanied by a decrease in net protein synthe- sis due to a decrease in transcription and translation of mRNAs, which, however, see their half-life increase (Van Breukelen and Martin, 2002). Hormonal changes that may account for the reorientation of interme- diary metabolism during the hibernation cycle have not been extensively studied to date, and the majority of data concerns fat-storing species and the regulation of glucose metabolism (see Table 1). An SP-induced Hormones and Behavior 64 (2013) 611–617 Abbreviations: SP, short photoperiod; LP, long photoperiod; RQ, respiratory quotient; WAT, white adipose tissue; GC, glucocorticoid; GLP-1, glucagon-like peptide 1; GiP, glucose dependant insulinotropic polypeptide. ⁎ Corresponding author at: Université de Strasbourg, IPHC-DEPE, 23 rue Becquerel, 67087 Strasbourg, France. Fax: +33 3 88 10 69 06. E-mail address: caroline.habold@iphc.cnrs.fr (C. Habold). 0018-506X/$ – see front matter © 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.yhbeh.2013.08.015 Contents lists available at ScienceDirect Hormones and Behavior journal homepage: www.elsevier.com/locate/yhbeh