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Free Radic Biol Med. 2013 Dec;65:916-924. doi: 10.1016/j.freeradbiomed.2013.08.188. Epub 2013 Sep 4.

The impact of cold acclimation and hibernation on antioxidant defenses in the ground squirrel (Spermophilus citellus): an update.

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University of Belgrade, Institute for Biological Research "Sinisa Stankovic," Department of Physiology, Bulevar despota Stefana 142, 11060 Belgrade, Serbia.
University of Belgrade, Faculty of Biology, Center for Electron Microscopy, Belgrade, Serbia.
Carleton University, Department of Biology, Ottawa, Ontario, Canada.
University of Belgrade, Institute for Biological Research "Sinisa Stankovic," Department of Physiology, Bulevar despota Stefana 142, 11060 Belgrade, Serbia. Electronic address:


Any alteration in oxidative metabolism is coupled with a corresponding response by an antioxidant defense (AD) in appropriate subcellular compartments. Seasonal hibernators pass through circannual metabolic adaptations that allow them to either maintain euthermy (cold acclimation) or enter winter torpor with body temperature falling to low values. The present study aimed to investigate the corresponding pattern of AD enzyme protein expressions associated with these strategies in the main tissues involved in whole animal energy homeostasis: brown and white adipose tissues (BAT and WAT, respectively), liver, and skeletal muscle. European ground squirrels (Spermophilus citellus) were exposed to low temperature (4 ± 1 °C) and then divided into two groups: (1) animals fell into torpor (hibernating group) and (2) animals stayed active and euthermic for 1, 3, 7, 12, or 21 days (cold-exposed group). We examined the effects of cold acclimation and hibernation on the tissue-dependent protein expression of four enzymes which catalyze the two-step detoxification of superoxide to water: superoxide dismutase 1 and 2 (SOD 1 and 2), catalase (CAT), and glutathione peroxidase (GSH-Px). The results showed that hibernation induced an increase of AD enzyme protein expressions in BAT and skeletal muscle. However, AD enzyme contents in liver were largely unaffected during torpor. Under these conditions, different WAT depots responded by elevating the amounts of specific enzymes, as follows: SOD 1 in retroperitoneal WAT, GSH-Px in gonadal WAT, and CAT in subcutaneous WAT. Similar perturbations of AD enzymes contents were seen in all tissues during cold acclimation, often in a time-dependent manner. It can be concluded that BAT and muscle AD capacity undergo the most dramatic changes during both cold acclimation and hibernation, while liver is relatively unaffected by either condition. Additionally, this study provides a basis for further metabolic study that will illuminate the causes of these tissue-specific AD responses, particularly the novel finding of distinct responses by different WAT depots in hibernators.


AD; Antioxidant; BAT; CAT; Cold acclimation; GSH-Px; H(2)O(2); Hibernation; O(2)(-); ROS; SOD; WAT; antioxidant defense; brown adipose tissue; catalase; glutathione peroxidase; gnWAT; gonadal WAT; hydrogen peroxide; reactive oxygen species; retroperitoneal WAT; rpWAT; scWAT; subcutaneous WAT; superoxide anion radical; superoxide dismutase; white adipose tissue

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