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

Vučetić, Milica; Stančić, Ana; Otašević, Vesna; Janković, Aleksandra; Korać, Aleksandra; Markelić, Milica; Veličković, Ksenija; Golić, Igor; Buzadžić, Biljana; Storey, Kenneth B.; Korać, Bato

doi:10.1016/j.freeradbiomed.2013.08.188

Cited by 45 publications

(39 citation statements)

References 59 publications

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“…While similar correlations were not observed during interbout arousal, or in liver or white adipose tissue during late torpor, the observed decrease in levels of SOD2 K68 acetylation still supports the general notion of increased antioxidant activity in these tissues as a result of differential acetylation, be it mediated by SIRTs or otherwise. Previous studies have also provided evidence of a role for increased SOD2 activity in the tissues of mammalian hibernators [3,44], but the current results represent the first support for differential acetylation acting as a possible mechanism for promoting SOD2 activity in this context. Similar conclusions were also drawn for the NF-jB subunit p65.…”

Section: Discussionsupporting

confidence: 59%

“…By extension, this would likely indicate that some of the metabolic and protective functions of SIRT3 are also relevant in this tissue during torpor. A SIRT3-mediated regulation of processes that reduce oxidative stress, for example, would serve a useful role in skeletal muscle during this time, when antioxidant responses are also known to be active in torpid tissues to prevent irreversible cellular damage at low temperatures, and to prepare for the drastic increases in oxygen consumption/ROS production that occur during arousal [3,12,31,44]. Similarly, the apparent upregulation of SIRT1 during arousal in liver and BAT may serve similar roles in promoting protective responses in the face of the increased oxygen stress that characterizes this transitory period, given that SIRT1 expression is known to induce resistance to oxidative stress [2].…”

Section: Discussionmentioning

confidence: 99%

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Characterization of the SIRT family of NAD+-dependent protein deacetylases in the context of a mammalian model of hibernation, the thirteen-lined ground squirrel

Rouble

Storey

2015

Cryobiology

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Section: Discussionsupporting

confidence: 59%

Section: Discussionmentioning

confidence: 99%

Characterization of the SIRT family of NAD+-dependent protein deacetylases in the context of a mammalian model of hibernation, the thirteen-lined ground squirrel

Rouble

Storey

2015

Cryobiology

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“…How mammalian hibernators are able to adapt to rapidly fluctuating oxygen levels without incurring oxidative damage, and how they avoid reperfusion injury in the brain and other sensitive tissues, is not well understood. Multiple studies have shown that hibernators display resistance to ischemia/reperfusion injury and, during torpor, increase expression of molecules that help regulate oxidative stress, such as superoxide dismutase 1 and 2, catalase, and glutathione peroxidase (2,(43)(44)(45)(46). Interestingly, uncoupling proteins have been linked to reduction of reactive oxygen species formation (47).…”

Section: Discussionmentioning

confidence: 99%

Neuronal UCP1 expression suggests a mechanism for local thermogenesis during hibernation

Laursen

Mastrotto

Pesta

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Hibernating mammals possess a unique ability to reduce their body temperature to ambient levels, which can be as low as −2.9°C, by active down-regulation of metabolism. Despite such a depressed physiologic phenotype, hibernators still maintain activity in their nervous systems, as evidenced by their continued sensitivity to auditory, tactile, and thermal stimulation. The molecular mechanisms that underlie this adaptation remain unknown. We report, using differential transcriptomics alongside immunohistologic and biochemical analyses, that neurons from thirteen-lined ground squirrels (Ictidomys tridecemlineatus) express mitochondrial uncoupling protein 1 (UCP1). The expression changes seasonally, with higher expression during hibernation compared with the summer active state. Functional and pharmacologic analyses show that squirrel UCP1 acts as the typical thermogenic protein in vitro. Accordingly, we found that mitochondria isolated from torpid squirrel brain show a high level of palmitate-induced uncoupling. Furthermore, torpid squirrels during the hibernation season keep their brain temperature significantly elevated above ambient temperature and that of the rest of the body, including brown adipose tissue. Together, our findings suggest that UCP1 contributes to local thermogenesis in the squirrel brain, and thus supports nervous tissue function at low body temperature during hibernation.T hirteen-lined ground squirrels (Ictidomys tridecemlineatus) are obligatory hibernating mammals. They are found across a wide range of latitudes, from southern Canada to the Gulf of Mexico. In northern habitats with long winters and limited food resources, ground squirrels breed only once a year, in late spring, and then hibernate in underground burrows from October to April. Hibernation consists of cycling between bouts of torpor and brief interbout arousal periods, each usually lasting less than 24 h (1, 2).During the long hibernation season, torpid animals undergo dramatic perturbations, including reduction in heart, respiratory, and overall metabolic rates, as well as decreases in core body temperature from 37°C to just above ambient temperature (often as low as 1-5°C) (2). Despite such a depressed physiologic phenotype, torpid animals remain sensitive to their environment (3). For example, during extreme winters, when ambient burrow temperatures reach the freezing point of water, most hibernating mammals increase metabolic activity and warm up as a safety precaution to prevent freezing (4). Similarly, arousal can be triggered by sound, touch, or a sudden increase in ambient temperature (3, 5). Thus, hibernating animals maintain activity in their peripheral and central nervous systems. Indeed, physiologic experiments conducted on nerve fibers isolated from torpid hamsters and squirrels demonstrated the ability to generate action potentials at temperatures prohibitively low for their nonhibernating relatives (i.e., rats, mice) (6-8).Deeply hibernating animals can keep their brain temperatures elevated above ambient by seve...

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“…As a proton pump, UCP-2 decreases the inner membrane potential of mitochondria and, with mild depolarization, reduces the production of reactive oxygen species [23,24], suggesting that its greatest role in the heart would be as an antioxidant. More importantly, the antioxidant status of many tissues in animals that are in the hibernating state appears protected, as demonstrated by increased expression of additional proteins including catalase, superoxide dismutase [1,2], and glutathione peroxidase [25,26]. In fact, the activities of several antioxidant enzymes have been shown to be increased during hibernating states [27] and, in European ground squirrels, include enhanced activities of superoxide dismutase, ascorbate, and glutathione peroxidase [28].…”

Section: Antioxidant Proteins From Hibernating Hearts In Naturementioning

confidence: 99%

The Recovery of Hibernating Hearts Lies on a Spectrum: from Bears in Nature to Patients with Coronary Artery Disease

Colbert

Holley

Stone

et al. 2015

J. of Cardiovasc. Trans. Res.

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Clinicians often use the term "hibernating myocardium" in reference to patients with ischemic heart disease and decreased function within viable myocardial regions. Because the term is a descriptor of nature's process of torpor, we provide a comparison of the adaptations observed in both conditions. In nature, hearts from hibernating animals undergo a shift in substrate preference in favor of fatty acids, while preserving glucose uptake and glycogen. Expression of electron transport chain proteins in mitochondria is decreased while antioxidant proteins including uncoupling protein-2 are increased. Similarly, hibernating hearts from patients have a comparable metabolic signature, with increased glucose uptake and glycogen accumulation and decreased oxygen consumption. In contrast to nature however, patients with hibernating hearts are at increased risk for arrhythmias, and contractility does not fully recover following revascularization. Clearly, additional interventions need to be advanced in patients with coronary artery disease and hibernating myocardium to prevent refractory heart failure.

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

Cited by 45 publications

References 59 publications

Characterization of the SIRT family of NAD+-dependent protein deacetylases in the context of a mammalian model of hibernation, the thirteen-lined ground squirrel

Characterization of the SIRT family of NAD+-dependent protein deacetylases in the context of a mammalian model of hibernation, the thirteen-lined ground squirrel

Neuronal UCP1 expression suggests a mechanism for local thermogenesis during hibernation

The Recovery of Hibernating Hearts Lies on a Spectrum: from Bears in Nature to Patients with Coronary Artery Disease

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