Physiological oxidative stress after arousal from hibernation in Arctic ground squirrel

Orr, Adrienne; Lohse, Lonita A.; Drew, Kelly L.; Hermes‐Lima, Marcelo

doi:10.1016/j.cbpa.2009.02.016

Cited by 98 publications

(85 citation statements)

References 41 publications

(94 reference statements)

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“…Hibernation produces rapid changes in body temperature and oxidative stress during reperfusion (17,67). Damaged cellular proteins can be repaired by chaperone and heat shock proteins or ubiquitinated and hydrolyzed by the proteasome.…”

Section: Discussionmentioning

confidence: 99%

Effects of hibernation on bone marrow transcriptome in thirteen-lined ground squirrels

Cooper

Sell

Fahrenkrog

et al. 2016

Physiological Genomics

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M. Effects of hibernation on bone marrow transcriptome in thirteen-lined ground squirrels. Physiol Genomics 48: 513-525, 2016. First published May 20, 2016 doi:10.1152/physiolgenomics.00120.2015.-Mammalian hibernators adapt to prolonged periods of immobility, hypometabolism, hypothermia, and oxidative stress, each capable of reducing bone marrow activity. In this study bone marrow transcriptomes were compared among thirteen-lined ground squirrels collected in July, winter torpor, and winter interbout arousal (IBA). The results were consistent with a suppression of acquired immune responses, and a shift to innate immune responses during hibernation through higher complement expression. Consistent with the increase in adipocytes found in bone marrow of hibernators, expression of genes associated with white adipose tissue are higher during hibernation. Genes that should strengthen the bone by increasing extracellular matrix were higher during hibernation, especially the collagen genes. Finally, expression of heat shock proteins were lower, and cold-response genes were higher, during hibernation. No differential expression of hematopoietic genes involved in erythrocyte or megakaryocyte production was observed. This global view of the changes in the bone marrow transcriptome over both short term (torpor vs. IBA) and long term (torpor vs. July) hypothermia can explain several observations made about circulating blood cells and the structure and strength of the bone during hibernation. erythrocyte; leukocyte; megakaryocyte; osteoblast; adipose BONE MARROW IS A COMPLEX ORGAN consisting of many different cell types and stem cell pools. These cells express both unique and common sets of genes and likely influence each other's activities. Hematopoietic stem cells can differentiate into lymphoid progenitor cells that produce natural killer cells and lymphocytes, or into myeloid progenitor cells that give rise to erythrocytes, the remaining leukocytes, and megakaryocytes. Megakaryocytes in turn shed anucleated platelets involved in blood clotting and inflammation. Bone marrow resident mesenchymal stem cells can differentiate to produce resident bone cells including osteoblasts, adipocytes, and chondrocytes (64). Osteoblasts can terminally differentiate into osteocytes and are involved in maintaining bone strength and extracellular matrix production. Bone marrow adipose composition is affected by age, diet, and disease states. Bone marrow may also contain skeletal muscle and hepatocyte stem cell pools. Because of the rapid rate of mitosis by multiple resident stem cell pools, bone marrow is sensitive to damage by radiation and chemotherapy, leaving patients immunocompromised and anemic (25). Bone mineral density and collagen are decreased by prolonged disuse such as bed rest or immobilization (45,86). Recent studies have also demonstrated an increase in neutrophils, natural killer cells, and lymphocytes and a decrease in monocytes in patients subjected to 60 days of bed rest (38). Finally, bone marrow adipocytes increase in ...

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Section: Discussionmentioning

confidence: 99%

Effects of hibernation on bone marrow transcriptome in thirteen-lined ground squirrels

Cooper

Sell

Fahrenkrog

et al. 2016

Physiological Genomics

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“…However, there is evidence that levels of antioxidant metabolites are elevated; for example, ascorbate levels rise 3-to 5-fold in plasma during torpor and ascorbate is redistributed from plasma to liver and spleen tissues, at the same time as oxygen consumption peaks, during arousal from torpor in Arctic ground squirrels (Tøien et al, 2001;Drew et al, 2002). Elevated levels of oxidative stress markers were reported in brown adipose tissue (but not liver) of Arctic ground squirrels during arousal compared with torpor (Orr et al, 2009) indicating that this thermogenic organ experiences ROS challenge during arousal. As skeletal muscle is the other thermogenic tissue that powers arousal, enhanced antioxidant capacity in the muscle of torpid animals would be a valuable preparation for muscle to deal with oxidative stress during arousal.…”

Section: Antioxidantsmentioning

confidence: 98%

The effects of hibernation on the contractile and biochemical properties of skeletal muscles in the thirteen-lined ground squirrel, Ictidomys tridecemlineatus

James

Staples

Brown

et al. 2013

Journal of Experimental Biology

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SUMMARYHibernation is a crucial strategy of winter survival used by many mammals. During hibernation, thirteen-lined ground squirrels, Ictidomys tridecemlineatus, cycle through a series of torpor bouts, each lasting more than a week, during which the animals are largely immobile. Previous hibernation studies have demonstrated that such natural models of skeletal muscle disuse cause limited or no change in either skeletal muscle size or contractile performance. However, work loop analysis of skeletal muscle, which provides a realistic assessment of in vivo power output, has not previously been undertaken in mammals that undergo prolonged torpor during hibernation. In the present study, our aim was to assess the effects of 3months of hibernation on contractile performance (using the work loop technique) and several biochemical properties that may affect performance. There was no significant difference in soleus muscle power output-cycle frequency curves between winter (torpid) and summer (active) animals. Total antioxidant capacity of gastrocnemius muscle was 156% higher in torpid than in summer animals, suggesting one potential mechanism for maintenance of acute muscle performance. Soleus muscle fatigue resistance was significantly lower in torpid than in summer animals. Gastrocnemius muscle glycogen content was unchanged. However, state 3 and state 4 mitochondrial respiration rates were significantly suppressed, by 59% and 44%, respectively, in mixed hindlimb skeletal muscle from torpid animals compared with summer controls. These findings in hindlimb skeletal muscles suggest that, although maximal contractile power output is maintained in torpor, there is both suppression of ATP production capacity and reduced fatigue resistance.

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“…As body mass loss of torpor-reluctant individuals was not in a critical range, it is more likely that the benefits of torpor use might just not have outweighed its advantages for these individuals. Although the potential benefits of torpor use are diverse (Geiser and Brigham, 2012), torpor use also comes with costs, such as slowed reactions (Rojas et al, 2012) and increased oxidative stress (Carey et al, 2000; but see Orr et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

Friends with benefits: the role of huddling in mixed groups of torpid and normothermic animals

Nowack

Geiser

2015

Journal of Experimental Biology

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Huddling and torpor are widely used for minimizing heat loss by mammals. Despite the questionable energetic benefits from social heterothermy of mixed groups of warm normothermic and cold torpid individuals, the heterothermic Australian sugar glider (Petaurus breviceps) rests in such groups during the cold season. To unravel why they might do so, we examined torpor expression of two sugar glider groups of four individuals each in outside enclosures during winter. We observed 79 torpor bouts during 50 days of observation and found that torpor bouts were longer and deeper when all individuals of a group entered torpor together, and therefore infer that they would have saved more energy in comparison to short and shallow solitary torpor bouts. However, all gliders of either group only expressed torpor uniformly in response to food restriction, whereas on most occasions at least one individual per group remained normothermic. Nevertheless, the presence of warm gliders in mixed groups also appears to be of energetic advantage for torpid individuals, because nest box temperature was negatively correlated with the number of torpid gliders, and normothermic individuals kept the nest temperature at a value closer to the threshold for thermoregulatory heat production during torpor. Our study suggests that mixed groups of torpid and normothermic individuals are observed when environmental conditions are adverse but food is available, leading to intermediate energy savings from torpor. However, under especially challenging conditions and when animals are starving, energy savings are maximized by uniform and pronounced expression of torpor.

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Physiological oxidative stress after arousal from hibernation in Arctic ground squirrel

Cited by 98 publications

References 41 publications

Effects of hibernation on bone marrow transcriptome in thirteen-lined ground squirrels

Effects of hibernation on bone marrow transcriptome in thirteen-lined ground squirrels

The effects of hibernation on the contractile and biochemical properties of skeletal muscles in the thirteen-lined ground squirrel, Ictidomys tridecemlineatus

Friends with benefits: the role of huddling in mixed groups of torpid and normothermic animals

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