Biomarker-based assessment of the muscle maintenance and energy status of anurans from an extremely seasonal semi-arid environment, the Brazilian Caatinga
Abstract:Biomarker-based assessment of the muscle maintenance and energy status of anurans from an extremely seasonal semi-arid environment, the Brazillian Caatinga
“…It corroborates with the finding in aestivating anurans ( Cyclorana and Neobatrachus ) by Saymour (1973) , Withers (1993) , and Withers and Thompson (2000) with respect to decreased oxygen consumption and thyroid activity. Several studies have reported significant depression in aerobic metabolism rate during winter dormancy and aestivation in different anurans ( Storey and Storey, 1996 ; Hudson et al, 2006 ; Madelaire et al, 2020 ; Moreira et al, 2020 ). Unlike some anurans who endure dormancy in a hypoxic microhabitat and undergo anaerobic metabolic depression ( Rossi et al, 2020 ), toads like Sacphiopus couchii and frogs like Pleuroderma diplolistris , and Proceratophrys cristiceps follow aerobic metabolic depression in almost a normoxic microhabitat with air-filled chambers in sandy soil ( Seymour, 1973 ; Flanigan et al, 1990 ; Cervalho et al, 2010 ; Moreira et al, 2020 ).…”
To assess redox status during hibernation with metabolic depression, oxidative stress parameters and antioxidant defense were assessed during different phases of hibernation including active period, hibernation, arousal, and post arousal period, in the liver and brain tissues of Duttaphrynus melanostictus. We hypothesized low levels of oxidative stress and antioxidant defense during the hibernation period in comparison to the summer active period due to hypometabolism and their subsequent increase during the arousal period following an increase in body temperature and metabolism. Contrary to our hypothesis increased oxidative stress with significantly higher lipid peroxidation, protein carbonylation, GSSG/GSH ratio, and elevated antioxidants defense consisting of higher catalase activity and high ascorbic acid content to control oxidative stress were found during hibernation. However, GSH and uric acid levels were found low with SOD activities at a steady level during hibernation. Supporting our hypothesis increased oxidative stress with high lipid peroxidation and GSSG/GSH ratio were found during arousal from hibernation owing to increased oxygen consumption and rewarming. Augmented catalase and SOD activities and nonenzymatic antioxidants (GSH, ascorbic acid, and uric acid) level were found to counteract oxidative stress during arousal periods as it was expected. A steady level of protein carbonylation indicating no oxidative damage during arousal from hibernation due to elevated antioxidant defense shows the significance of hibernation to overcome food and water scarcity and cold climatic condition. Decrease in antioxidants levels accompanying coming down of lipid peroxidation, protein carbonylation, and GSSG/GSH ratio to their lower levels during post arousal period showing normalcy in redox status as it was during active period indicates controllability of oxidative stress in hibernating toads.
“…It corroborates with the finding in aestivating anurans ( Cyclorana and Neobatrachus ) by Saymour (1973) , Withers (1993) , and Withers and Thompson (2000) with respect to decreased oxygen consumption and thyroid activity. Several studies have reported significant depression in aerobic metabolism rate during winter dormancy and aestivation in different anurans ( Storey and Storey, 1996 ; Hudson et al, 2006 ; Madelaire et al, 2020 ; Moreira et al, 2020 ). Unlike some anurans who endure dormancy in a hypoxic microhabitat and undergo anaerobic metabolic depression ( Rossi et al, 2020 ), toads like Sacphiopus couchii and frogs like Pleuroderma diplolistris , and Proceratophrys cristiceps follow aerobic metabolic depression in almost a normoxic microhabitat with air-filled chambers in sandy soil ( Seymour, 1973 ; Flanigan et al, 1990 ; Cervalho et al, 2010 ; Moreira et al, 2020 ).…”
To assess redox status during hibernation with metabolic depression, oxidative stress parameters and antioxidant defense were assessed during different phases of hibernation including active period, hibernation, arousal, and post arousal period, in the liver and brain tissues of Duttaphrynus melanostictus. We hypothesized low levels of oxidative stress and antioxidant defense during the hibernation period in comparison to the summer active period due to hypometabolism and their subsequent increase during the arousal period following an increase in body temperature and metabolism. Contrary to our hypothesis increased oxidative stress with significantly higher lipid peroxidation, protein carbonylation, GSSG/GSH ratio, and elevated antioxidants defense consisting of higher catalase activity and high ascorbic acid content to control oxidative stress were found during hibernation. However, GSH and uric acid levels were found low with SOD activities at a steady level during hibernation. Supporting our hypothesis increased oxidative stress with high lipid peroxidation and GSSG/GSH ratio were found during arousal from hibernation owing to increased oxygen consumption and rewarming. Augmented catalase and SOD activities and nonenzymatic antioxidants (GSH, ascorbic acid, and uric acid) level were found to counteract oxidative stress during arousal periods as it was expected. A steady level of protein carbonylation indicating no oxidative damage during arousal from hibernation due to elevated antioxidant defense shows the significance of hibernation to overcome food and water scarcity and cold climatic condition. Decrease in antioxidants levels accompanying coming down of lipid peroxidation, protein carbonylation, and GSSG/GSH ratio to their lower levels during post arousal period showing normalcy in redox status as it was during active period indicates controllability of oxidative stress in hibernating toads.
“…Circulating levels of androgens, corticosterone, and leukocytes, as well as the inflammatory response to immunological challenges, are suppressed during the dry season ( Madelaire and Gomes, 2016 ; Madelaire et al, 2017 ). More recently, adjustments in the regulation of energy turnover, protein synthesis, and proteostasis in the skeletal muscle of P. diplolister during estivation have also been described ( Madelaire et al, 2020 ). In brief, key biomarkers indicate the maintenance of aerobic capacity, suppression of protein synthesis, and activation of cell survival processes in the muscle of P. diplolister during the dry season ( Madelaire et al, 2020 ).…”
Section: Introductionmentioning
confidence: 99%
“…More recently, adjustments in the regulation of energy turnover, protein synthesis, and proteostasis in the skeletal muscle of P. diplolister during estivation have also been described ( Madelaire et al, 2020 ). In brief, key biomarkers indicate the maintenance of aerobic capacity, suppression of protein synthesis, and activation of cell survival processes in the muscle of P. diplolister during the dry season ( Madelaire et al, 2020 ). These findings were interpreted as a strategy to limit the loss of musculoskeletal performance despite the long period of inactivity and lack of environmental resources ( Madelaire et al, 2020 ).…”
Section: Introductionmentioning
confidence: 99%
“…In brief, key biomarkers indicate the maintenance of aerobic capacity, suppression of protein synthesis, and activation of cell survival processes in the muscle of P. diplolister during the dry season ( Madelaire et al, 2020 ). These findings were interpreted as a strategy to limit the loss of musculoskeletal performance despite the long period of inactivity and lack of environmental resources ( Madelaire et al, 2020 ). Indeed, estivating anurans are extraordinarily resistant to muscle atrophy ( Hudson and Franklin, 2002 ; Hudson et al, 2006 ; Reilly and Franklin, 2016 ), whose underlying mechanism has a strong contribution of reactive oxygen species and antioxidant systems ( Powers et al, 2011 ; Talbert et al, 2013 ).…”
The upregulation of endogenous antioxidants (i.e., preparation for oxidative stress, POS) is part of the biochemical responses underlying the adaptation of animals to adverse environments. Despite the phylogenetic diversity of animals in which POS has been described, most studies focus on animals under controlled laboratory conditions. To address this limitation, we have recently assessed the redox metabolism in the skeletal muscle of Proceratophrys cristiceps estivating under natural settings in the Caatinga. Here, we analyzed biochemical biomarkers in the muscle of another Caatinga species, Pleurodema diplolister, during the rainy (active) and dry (estivating frogs) seasons. We aimed to determine whether P. diplolister enhances its antioxidants during estivation under field conditions and to identify any effect of species on the biochemical responses of P. diplolister and P. cristiceps associated with estivation. To do so, we measured the activities of representative enzymes of intermediary metabolism and antioxidant systems, as well as glutathione and protein carbonyl levels, in the skeletal muscle of P. diplolister. Our findings revealed the suppression of oxidative metabolism and activation of antioxidant enzymes in estivating P. diplolister compared with active specimens. No changes in oxidative damage to proteins were observed and estivating P. diplolister had lower levels of disulfide glutathione (GSSG) and disulfide-to-total glutathione ratio (GSSG/tGSH) than those observed in active individuals. When data for P. diplolister and P. cristiceps were assembled and analyzed, significant effects of species were detected on the activities of metabolic enzymes (citrate synthase, isocitric dehydrogenase, malic enzyme, and creatine kinase) and antioxidant enzymes (catalase, glutathione peroxidase and glutathione transferase), as well as on GSSG/tGSH ratio. Such effects might underlie the physiological and behavioral differences between these two species that share the same microhabitat and survival strategy (i.e., to estivate) during the dry season. Despite some peculiarities, which reflect the physiological diversity of the mechanisms associated with estivation in the Brazilian Caatinga, both P. diplolister and P. cristiceps seem to balance the suppression of oxidative pathways, the maintenance of the capacity of oxygen-independent pathways, and the activation of endogenous antioxidants to preserve muscle function and be ready to resume activity whenever the unpredictable rainy period arrives.
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