Lauren de Wit, Maarten R Hamberg, Anne M Ross, Maaike Goris, Fia F Lie, Thomas Ruf, Sylvain Giroud, Robert H Henning, Roelof A Hut
{"title":"Temperature Effects on DNA Damage during Hibernation.","authors":"Lauren de Wit, Maarten R Hamberg, Anne M Ross, Maaike Goris, Fia F Lie, Thomas Ruf, Sylvain Giroud, Robert H Henning, Roelof A Hut","doi":"10.1086/722904","DOIUrl":"10.1086/722904","url":null,"abstract":"<p><p>AbstractDuring multiday torpor, deep-hibernating mammals maintain a hypometabolic state where heart rate and ventilation are reduced to 2%-4% of euthermic rates. It is hypothesized that this ischemia-like condition may cause DNA damage through reactive oxygen species production. The reason for intermittent rewarming (arousal) during hibernation might be to repair the accumulated DNA damage. Because increasing ambient temperatures (<i>T</i><sub>a</sub>'s) shortens torpor bout duration, we hypothesize that hibernating at higher <i>T</i><sub>a</sub>'s will result in a faster accumulation of genomic DNA damage. To test this, we kept 39 male and female garden dormice at a <i>T</i><sub>a</sub> of either 5°C or 10°C and obtained tissue at 1, 4, and 8 d in torpor to assess DNA damage and recruitment of DNA repair markers in splenocytes. DNA damage in splenocytes measured by comet assay was significantly higher in almost all torpor groups than in summer euthermic groups. Damage accumulates in the first days of torpor at <math><mrow><msub><mrow><mi>T</mi></mrow><mrow><mi>a</mi></mrow></msub><mo>=</mo><msup><mrow><mn>5</mn></mrow><mrow><mo>°</mo></mrow></msup><mtext>C</mtext></mrow></math> (between days 1 and 4) but not at <math><mrow><msub><mrow><mi>T</mi></mrow><mrow><mi>a</mi></mrow></msub><mo>=</mo><msup><mrow><mn>10</mn></mrow><mrow><mo>°</mo></mrow></msup><mtext>C</mtext></mrow></math>. At the higher <i>T</i><sub>a</sub>, DNA damage is high at 24 h in torpor, indicating either a faster buildup of DNA damage at higher <i>T</i><sub>a</sub>'s or an incomplete repair during arousals in dormice. At 5°C, recruitment of the DNA repair protein 53BP1 paralleled the increase in DNA damage over time during torpor. In contrast, after 1 d in torpor at 10°C, DNA damage levels were high, but 53BP1 was not recruited to the nuclear DNA yet. The data suggest a potential mismatch in the DNA damage/repair dynamics during torpor at higher <i>T</i><sub>a</sub>'s.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.8,"publicationDate":"2023-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9191677","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Thermal Stability of Contractile Proteins in Bat Wing Muscles Explains Differences in Temperature Dependence of Whole-Muscle Shortening Velocity.","authors":"Andrea D Rummel, Sharon M Swartz, Richard L Marsh","doi":"10.1086/722449","DOIUrl":"https://doi.org/10.1086/722449","url":null,"abstract":"<p><p>AbstractMuscle contractile properties are dependent on temperature: cooler temperatures generally slow contractile rates. Contraction and relaxation are driven by underlying biochemical systems, which are inherently sensitive to temperature. <i>Carollia perspicillata</i>, a small Neotropical bat, experiences large temperature differentials among body regions, resulting in a steep gradient in temperature along the wing. Although the bats maintain high core body temperatures during flight, the wing muscles may operate at more than 10°C below body temperature. Partially compensating for these colder operating temperatures, distal wing muscles have lower temperature sensitivities in their contractile properties, including shortening velocity, relative to the proximal pectoralis. Shortening velocity is correlated with the activity of myosin ATPase, an enzyme that drives the cross-bridge cycle. We hypothesized that the thermal properties of myofibrillar ATPase from the pectoralis and forearm muscles of the bat wing would correlate with the temperature sensitivity of those muscles. Using myofibrillar ATPases from the proximal and distal muscles, we measured enzyme activity across a range of temperatures and enzyme thermal stability after heat incubation across a range of time points. We found that forearm muscle myofibrillar ATPase was significantly less thermally stable than pectoralis myofibrillar ATPase but that there was no significant difference in the acute temperature dependence of enzyme activity between the two muscles.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2023-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9191670","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Michael D Treat, Anthony J Marlon, Frank van Breukelen
{"title":"Incomplete Caspase 3 Activation and Mitigation of Apoptosis in Hibernating Ground Squirrels, <i>Spermophilus lateralis</i>.","authors":"Michael D Treat, Anthony J Marlon, Frank van Breukelen","doi":"10.1086/722708","DOIUrl":"https://doi.org/10.1086/722708","url":null,"abstract":"<p><p>AbstractHibernating golden-mantled ground squirrels, <i>Spermophilus [Callospermophilus] lateralis</i>, tolerate proapoptotic conditions, such as low body temperature, anorexia, acidosis, and ischemia/reperfusion. Avoiding widespread apoptosis is critical for hibernator survival. Caspase 3, the key executioner of apoptosis, cleaves a majority of apoptotic targets. Under proapoptotic conditions, inactive procaspase 3 (32 kDa) is activated when cleaved into 17- and 12-kDa fragments (p32, p17, and p12, respectively). Caspase 3 activation results in extreme enzymatic activation. Activity increases >10,000-fold followed by apoptotic execution. Is widespread apoptosis occurring during the proapoptotic hibernation season? Western blots showed p17 increased ∼2-fold during hibernation, indicating caspase 3 activation. However, in vitro caspase 3 activity assays found no extreme increases in activity. Downstream caspase 3 targets ICAD (inhibitor of caspase-activated deoxyribonuclease) and PARP (poly (ADP-ribose) polymerase) did not experience elevated cleavage during hibernation, which is inconsistent with caspase 3 activation. TUNEL (terminal deoxynucleotidyl transferase-mediated deoxyuridine triphosphate nick-end labeling) assays from multiple tissues found only 0.001%-0.009% of cells were TUNEL positive during winter, indicating negligible apoptosis during hibernation. Typically, caspase 3 activation generates a strong commitment toward apoptosis. We found that despite a ∼2-fold increase in active caspase 3, hibernators experience no downstream caspase 3 activity or widespread apoptosis. A systems-level approach suggests an incomplete signaling cascade wherein some caspase 3 activation during hibernation does not necessarily lead to bona fide apoptosis.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2023-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9197185","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Henry S Pollock, Daniel Lamont, Sean E MacDonald, Austin R Spence, Jeffrey D Brawn, Zachary A Cheviron
{"title":"Widespread Torpor Use in Hummingbirds from the Thermally Stable Lowland Tropics.","authors":"Henry S Pollock, Daniel Lamont, Sean E MacDonald, Austin R Spence, Jeffrey D Brawn, Zachary A Cheviron","doi":"10.1086/722477","DOIUrl":"https://doi.org/10.1086/722477","url":null,"abstract":"<p><p>AbstractTorpor, the temporary reduction of metabolic rate and body temperature, is a common energy-saving strategy in endotherms. Because of their small body size and energetically demanding life histories, hummingbirds have proven useful for understanding when and why endotherms use torpor. Previous studies of torpor in hummingbirds have been largely limited to tropical montane species or long-distance migrants that regularly experience challenging thermal conditions. Comparatively little is known, however, about the use of torpor in hummingbirds of the lowland tropics, where relatively high and stable year-round temperatures may at least partially negate the need for torpor. To fill this knowledge gap, we tested for the occurrence of torpor in tropical lowland hummingbirds (<math><mrow><mi>n</mi><mo>=</mo><mn>37</mn></mrow></math> individuals of six species) from central Panama. In controlled experimental conditions simulating the local temperature regime, all six species used torpor to varying degrees and entered torpor at high ambient temperatures (i.e., ≥28°C), indicating that hummingbirds from the thermally stable lowland tropics regularly use torpor. Torpor reduced overnight mass loss, with individuals that spent more time in torpor losing less body mass during temperature experiments. Body mass was the best predictor of torpor depth and duration among and within species-smaller species and individuals tended to use torpor more frequently and enter deeper torpor. Average mass loss in our experiments (∼8%-10%) was greater than that reported in studies of hummingbirds from higher elevation sites (∼4%). We therefore posit that the energetic benefits accrued from torpor may be limited by relatively high nighttime temperatures in the lowland tropics, although further studies are needed to test this hypothesis.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2023-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9191673","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Could Chronic Hypothermia in a Human Affect the Clock System?","authors":"André Malan, Gerhard Heldmaier","doi":"10.1086/722707","DOIUrl":"https://doi.org/10.1086/722707","url":null,"abstract":"<p><p>AbstractHibernation-like episodes would be particularly interesting for clinical and spatial use if they could be observed and induced in humans. As animal hibernation differs from hypothermia with its control by a temperature-dependent clock, we undertook to find evidence that human hypothermia might affect the circadian clock system. We revisited Siffre's 1962 abyss experiment. Deprived of temporal information and showing signs of chronic hypothermia, Siffre underestimated his stay underground by 22 d. We show that the temperature-dependent clock equation for classical hibernators accurately predicts Siffre's subjective times, and we list potential conditions to be further explored for inducing hibernation-like bouts in humans.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2023-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9197187","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Michael J Lawrence, Hanna Scheuffele, Stephen B Beever, Peter E Holder, Colin J Garroway, Steven J Cooke, Timothy D Clark
{"title":"The Role of Metabolic Phenotype in the Capacity to Balance Competing Energetic Demands.","authors":"Michael J Lawrence, Hanna Scheuffele, Stephen B Beever, Peter E Holder, Colin J Garroway, Steven J Cooke, Timothy D Clark","doi":"10.1086/722478","DOIUrl":"https://doi.org/10.1086/722478","url":null,"abstract":"<p><p>AbstractGiven the critical role of metabolism in the life history of all organisms, there is particular interest in understanding the relationship between individual metabolic phenotypes and the capacity to partition energy into competing life history traits. Such relationships could be predictive of individual phenotypic performances throughout life. Here, we were specifically interested in whether an individual fish's metabolic phenotype can shape its propensity to feed following a significant stressor (2-min exhaustive exercise challenge). Such a relationship would provide insight into previous intraspecific observations linking high metabolism with faster growth. Using a teleost fish, the barramundi (<i>Lates calcarifer</i>), we predicted that individuals with high standard metabolic rates (SMRs) and maximal metabolic rates (MMRs) would be faster to recover and resume feeding after exercise. Contrary to our prediction, neither SMR nor MMR was correlated with latency to feed after exercise (food was offered at 0.5, 1.5, 3, and 18 h after exercise). Only time after exercise and individual fish ID were significant predictors of latency to feed. Measurements of MMR from the same individuals (three measurements spaced 8-12 d apart) revealed a moderate degree of repeatability (<math><mrow><mi>R</mi><mo>=</mo><mn>0.319</mn></mrow></math>). We propose that interindividual differences in biochemical and endocrine processes may be more influential than whole-organism metabolic phenotype in mediating feeding latency after exercise.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2023-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9197189","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sara Kophamel, Leigh C Ward, Ellen Ariel, Diana Mendez, Lauren M O'Brien, Lauren Burchell, Suzanne L Munns
{"title":"A Standardized Protocol for Measuring Bioelectrical Impedance in Green Turtles (<i>Chelonia mydas</i>).","authors":"Sara Kophamel, Leigh C Ward, Ellen Ariel, Diana Mendez, Lauren M O'Brien, Lauren Burchell, Suzanne L Munns","doi":"10.1086/722451","DOIUrl":"https://doi.org/10.1086/722451","url":null,"abstract":"<p><p>AbstractBioelectrical impedance analysis (BIA) is gaining popularity in wildlife studies as a portable technology for immediate and nondestructive predictions of body composition components, such as fat-free and fat masses. Successful application of BIA for field-based research requires the identification and control of potential sources of error, as well as the creation of and adherence to a standardized protocol for measurement. The aim of our study was to determine sources of error and to provide a standardization protocol to improve measurement precision of BIA on juvenile green turtles (<i>Chelonia mydas</i>; <math><mrow><mi>n</mi><mo>=</mo><mn>35</mn></mrow></math>). We assessed the effects of altered environmental temperature (20°C-30°C), postprandial state (2-72 h), and time out of the water (2 h) on five impedance parameters (resistance at infinite frequency [<i>R</i><sub>inf</sub>], resistance at zero frequency [<i>R</i><sub>0</sub>], resistance at 50 kHz [<i>R</i><sub>50</sub>], phase angle at 50 kHz [PhA<sub>50</sub>], and intracellular resistance [<i>R</i><sub>i</sub>]) using a bioimpedance spectroscopy device. Technical reproducibility of measurements and interanimal variability were also assessed. We found an inverse exponential relationship between change in environmental temperature and impedance parameters <i>R</i><sub>inf</sub>, <i>R</i><sub>0</sub>, and <i>R</i><sub>50</sub>. Postprandial state significantly increased <i>R</i><sub>inf</sub> and <i>R</i><sub>i</sub> 72 h after feeding. BIA measurements were reproducible within individual juvenile green turtles at temperatures from 20°C to 30°C. Significant variation in impedance values was found between animals at all temperatures, sampling times, and postprandial states, but the relative differences (%) were small in magnitude. Our study suggests that measurement precision is improved by measuring animals at consistent environmental temperatures close to their preferred thermal range. We propose a standardized protocol of measurement conditions to facilitate laboratory and field use of BIA for body composition assessment studies in turtles.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2023-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9197186","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Back to the Womb: A Perinatal Perspective on Mammalian Hibernation.","authors":"Dominique Singer","doi":"10.1086/722905","DOIUrl":"https://doi.org/10.1086/722905","url":null,"abstract":"<p><p>AbstractThe idea of putting astronauts into a hibernation-like state during interplanetary spaceflights has sparked new interest in the evolutionary roots of hibernation and torpor. In this context, it should be noted that mammalian fetuses and neonates respond to the environmental challenges in the perinatal period with a number of physiological mechanisms that bear striking similarity to hibernation and torpor. These include three main points: first, prenatal deviation from the overall metabolic size relationship, which adapts the fetus to the low-oxygen conditions in the womb and corresponds to the metabolic reduction during hibernation and estivation; second, intranatal diving bradycardia in response to shortened O<sub>2</sub> supply during birth, comparable to the decrease in heart rate preceding the drop in body temperature upon entry into torpor; and third, postnatal onset of nonshivering thermogenesis in the brown adipose tissue, along with the increase in basal metabolic rate up to the level expected from body size, such as during arousal from hibernation. The appearance of hibernation-like adaptations in the perinatal period suggests that, conversely, hibernation and torpor may be composed of mechanisms shared by all mammals around birth. This hypothesis sheds new light on the origins of hibernation and supports its potential accessibility to nonhibernating species, including humans.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2023-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9197188","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}