Sıla Algül, Larissa M Dorsch, Oana Sorop, Aryan Vink, Michelle Michels, Cristobal G Dos Remedios, Michiel Dalinghaus, Daphne Merkus, Dirk J Duncker, Diederik W D Kuster, Jolanda van der Velden
{"title":"The microtubule signature in cardiac disease: etiology, disease stage, and age dependency.","authors":"Sıla Algül, Larissa M Dorsch, Oana Sorop, Aryan Vink, Michelle Michels, Cristobal G Dos Remedios, Michiel Dalinghaus, Daphne Merkus, Dirk J Duncker, Diederik W D Kuster, Jolanda van der Velden","doi":"10.1007/s00360-023-01509-1","DOIUrl":"10.1007/s00360-023-01509-1","url":null,"abstract":"<p><p>Employing animal models to study heart failure (HF) has become indispensable to discover and test novel therapies, but their translatability remains challenging. Although cytoskeletal alterations are linked to HF, the tubulin signature of common experimental models has been incompletely defined. Here, we assessed the tubulin signature in a large set of human cardiac samples and myocardium of animal models with cardiac remodeling caused by pressure overload, myocardial infarction or a gene defect. We studied levels of total, acetylated, and detyrosinated α-tubulin and desmin in cardiac tissue from hypertrophic (HCM) and dilated cardiomyopathy (DCM) patients with an idiopathic (n = 7), ischemic (n = 7) or genetic origin (n = 59), and in a pressure-overload concentric hypertrophic pig model (n = 32), pigs with a myocardial infarction (n = 28), mature pigs (n = 6), and mice (n = 15) carrying the HCM-associated MYBPC3<sub>2373insG</sub> mutation. In the human samples, detyrosinated α-tubulin was increased 4-fold in end-stage HCM and 14-fold in pediatric DCM patients. Acetylated α-tubulin was increased twofold in ischemic patients. Across different animal models, the tubulin signature remained mostly unaltered. Only mature pigs were characterized by a 0.5-fold decrease in levels of total, acetylated, and detyrosinated α-tubulin. Moreover, we showed increased desmin levels in biopsies from NYHA class II HCM patients (2.5-fold) and the pressure-overload pig model (0.2-0.3-fold). Together, our data suggest that desmin levels increase early on in concentric hypertrophy and that animal models only partially recapitulate the proliferated and modified tubulin signature observed clinically. Our data warrant careful consideration when studying maladaptive responses to changes in the tubulin content in animal models.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"581-595"},"PeriodicalIF":2.0,"publicationDate":"2023-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10533615/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10167642","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Janna L Crossley, Brandt Smith, Melissa Tull, Ruth M Elsey, Tobias Wang, Dane A Crossley
{"title":"Hypoxic incubation at 50% of atmospheric levels shifts the cardiovascular response to acute hypoxia in American alligators, Alligator mississippiensis.","authors":"Janna L Crossley, Brandt Smith, Melissa Tull, Ruth M Elsey, Tobias Wang, Dane A Crossley","doi":"10.1007/s00360-023-01510-8","DOIUrl":"10.1007/s00360-023-01510-8","url":null,"abstract":"<p><p>We designed a series of studies to investigate whether hypoxia (10% O<sub>2</sub>) from 20% of incubation to hatching, or from 20 to 50% of incubation, affects cardiovascular function when juvenile American alligators reached an age of 4-5 years compared to juveniles that were incubated in 21% O<sub>2</sub>. At this age, we measured blood flows in all the major arteries as well as heart rate, blood pressure, and blood gases in animals in normoxia and acute hypoxia (10% O<sub>2</sub> and 5% O<sub>2</sub>). In all three groups, exposure to acute hypoxia of 10% O<sub>2</sub> caused a decrease in blood O<sub>2</sub> concentration and an increase in heart rate in 4-5-year-old animals, with limited effects on blood flow in the major outflow vessels of the heart. In response to more acute hypoxia (5% O<sub>2</sub>), where blood O<sub>2</sub> concentration decreased even further, we measured increased heart rate and blood flow in the right aorta, subclavian artery, carotid artery, and pulmonary artery; however, blood flow in the left aorta either decreased or did not change. Embryonic exposure to hypoxia increased the threshold for eliciting an increase in heart rate indicative of a decrease in sensitivity. Alligators that had been incubated in hypoxia also had higher arterial PCO<sub>2</sub> values in normoxia, suggesting a reduction in ventilation relative to metabolism.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"545-556"},"PeriodicalIF":2.0,"publicationDate":"2023-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10116927","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}
Rachel Demers, Ryan S O'Connor, Audrey Le Pogam, Kevin G Young, Dominique Berteaux, Andrew Tam, François Vézina
{"title":"Born in the cold: contrasted thermal exchanges and maintenance costs in juvenile and adult snow buntings on their breeding and wintering grounds.","authors":"Rachel Demers, Ryan S O'Connor, Audrey Le Pogam, Kevin G Young, Dominique Berteaux, Andrew Tam, François Vézina","doi":"10.1007/s00360-023-01502-8","DOIUrl":"10.1007/s00360-023-01502-8","url":null,"abstract":"<p><p>Several species of passerines leave their nest with unfinished feather growth, resulting in lower feather insulation and increased thermoregulatory demands compared to adults. However, feather insulation is essential for avian species breeding at northern latitudes, where cold conditions or even snowstorms can occur during the breeding season. In altricial arctic species, increased heat loss caused by poor feather insulation during growth could be counter-adaptative as it creates additional energy demands for thermoregulation. Using flow-through respirometry, we compared resting metabolic rate at thermoneutrality (RMRt), summit metabolic rate (M<sub>sum</sub>) and heat loss (conductance) in adult and juvenile snow buntings on their summer and winter grounds. In summer, when buntings are in the Arctic, juveniles had a 12% higher RMRt, likely due to unfinished growth, and lost 14% more heat to the environment than adults. This pattern may result from juveniles fledging early to avoid predation at the cost of lower feather insulation. Surprisingly, an opposite pattern was observed at lower latitudes on their wintering grounds. Although they showed no difference in RMRt and M<sub>sum</sub>, adults were losing 12% more heat than juveniles. We suggest that this difference is due to poorer insulative property of plumage in adults stemming from energetic and time constraints encountered during their post-breeding molt. High plumage insulation in first-winter juvenile buntings could be adaptive to reduce thermoregulatory demands and maximize survival in the first winter of life, while adults could use behavioral strategies to compensate for their greater rate of heat loss.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"557-568"},"PeriodicalIF":2.0,"publicationDate":"2023-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9695227","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}
Pedro Goes Nogueira-de-Sá, José Eduardo Pereira Wilken Bicudo, José Guilherme Chaui-Berlinck
{"title":"Energy and time optimization during exit from torpor in vertebrate endotherms.","authors":"Pedro Goes Nogueira-de-Sá, José Eduardo Pereira Wilken Bicudo, José Guilherme Chaui-Berlinck","doi":"10.1007/s00360-023-01494-5","DOIUrl":"https://doi.org/10.1007/s00360-023-01494-5","url":null,"abstract":"<p><p>Torpor is used in small sized birds and mammals as an energy conservation trait. Considerable effort has been put towards elucidating the mechanisms underlying its entry and maintenance, but little attention has been paid regarding the exit. Firstly, we demonstrate that the arousal phase has a stereotyped dynamic: there is a sharp increase in metabolic rate followed by an increase in body temperature and, then, a damped oscillation in body temperature and metabolism. Moreover, the metabolic peak is around two-fold greater than the corresponding euthermic resting metabolic rate. We then hypothesized that either time or energy could be crucial variables to this event and constructed a model from a collection of first principles of physiology, control engineering and thermodynamics. From the model, we show that the stereotyped pattern of the arousal is a solution to save both time and energy. We extended the analysis to the scaling of the use of torpor by endotherms and show that variables related to the control system of body temperature emerge as relevant to the arousal dynamics. In this sense, the stereotyped dynamics of the arousal phase necessitates a certain profile of these variables which is not maintained as body size increases.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":"193 4","pages":"461-475"},"PeriodicalIF":2.0,"publicationDate":"2023-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10053967","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}
Matthew R J Morris, Sara J Smith, Jonathan Rosebush, Sean M Rogers
{"title":"Correction to: Mitochondrial volume density and evidence for its role in adaptive divergence in response to thermal tolerance in threespine stickleback.","authors":"Matthew R J Morris, Sara J Smith, Jonathan Rosebush, Sean M Rogers","doi":"10.1007/s00360-023-01496-3","DOIUrl":"https://doi.org/10.1007/s00360-023-01496-3","url":null,"abstract":"","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":"193 4","pages":"477"},"PeriodicalIF":2.0,"publicationDate":"2023-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9690616","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}
Jules B L Devaux, Chris P Hedges, Nigel Birch, Neill Herbert, Gillian M C Renshaw, Anthony J R Hickey
{"title":"Electron transfer and ROS production in brain mitochondria of intertidal and subtidal triplefin fish (Tripterygiidae).","authors":"Jules B L Devaux, Chris P Hedges, Nigel Birch, Neill Herbert, Gillian M C Renshaw, Anthony J R Hickey","doi":"10.1007/s00360-023-01495-4","DOIUrl":"https://doi.org/10.1007/s00360-023-01495-4","url":null,"abstract":"<p><p>While oxygen is essential for oxidative phosphorylation, O<sub>2</sub> can form reactive species (ROS) when interacting with electrons of mitochondrial electron transport system. ROS is dependent on O<sub>2</sub> pressure (PO<sub>2</sub>) and has traditionally been assessed in O<sub>2</sub> saturated media, PO<sub>2</sub> at which mitochondria do not typically function in vivo. Mitochondrial ROS can be significantly elevated by the respiratory complex II substrate succinate, which can accumulate within hypoxic tissues, and this is exacerbated further with reoxygenation. Intertidal species are repetitively exposed to extreme O<sub>2</sub> fluctuations, and have likely evolved strategies to avoid excess ROS production. We evaluated mitochondrial electron leakage and ROS production in permeabilized brain of intertidal and subtidal triplefin fish species from hyperoxia to anoxia, and assessed the effect of anoxia reoxygenation and the influence of increasing succinate concentrations. At typical intracellular PO<sub>2</sub>, net ROS production was similar among all species; however at elevated PO<sub>2</sub>, brain tissues of the intertidal triplefin fish released less ROS than subtidal species. In addition, following in vitro anoxia reoxygenation, electron transfer mediated by succinate titration was better directed to respiration, and not to ROS production for intertidal species. Overall, these data indicate that intertidal triplefin fish species better manage electrons within the ETS, from hypoxic-hyperoxic transitions.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":"193 4","pages":"413-424"},"PeriodicalIF":2.0,"publicationDate":"2023-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10299943/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9704700","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Investigating nitrogen movement in North Pacific spiny dogfish (Squalus acanthias suckleyi), with focus on UT, Rhp2, and Rhbg mRNA abundance.","authors":"J Lisa Hoogenboom, W Gary Anderson","doi":"10.1007/s00360-023-01487-4","DOIUrl":"10.1007/s00360-023-01487-4","url":null,"abstract":"<p><p>For ureosmotic marine elasmobranchs, the acquisition and retention of nitrogen is critical for the synthesis of urea. To better understand whole-body nitrogen homeostasis, we investigated mechanisms of nitrogen trafficking in North Pacific spiny dogfish (Squalus acanthias suckleyi). We hypothesized that the presence of nitrogen within the spiral valve lumen would affect both the transport of nitrogen and the mRNA abundance of a urea transporter (UT) and two ammonia transport proteins (Rhp2, Rhbg) within the intestinal epithelium. The in vitro preincubation of intestinal tissues in NH<sub>4</sub>Cl, intended to simulate dietary nitrogen availability, showed that increased ammonia concentrations did not significantly stimulate the net uptake of total urea or total methylamine. We also examined the mRNA abundance of UT, Rhp2, and Rhbg in the gills, kidney, liver, and spiral valve of fasted, fed, excess urea fed, and antibiotic-treated dogfish. After fasting, hepatic UT mRNA abundance was significantly lower, and Rhp2 mRNA in the gills was significantly higher than the other treatments. Feeding significantly increased Rhp2 mRNA levels in the kidney and mid spiral valve region. Both excess urea and antibiotics significantly reduced Rhbg mRNA levels along all three spiral valve regions. The antibiotic treatment also significantly diminished UT mRNA abundance levels in the anterior and mid spiral valve, and Rhbg mRNA levels in the kidney. In our study, no single treatment had significantly greater influence on the overall transcript abundance of the three transport proteins compared to another treatment, demonstrating the dynamic nature of nitrogen balance in these ancient fish.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":"193 4","pages":"439-451"},"PeriodicalIF":2.0,"publicationDate":"2023-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9696806","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}
Ercüment Aksakal, Ercan Soydan, Abdullah Tunç, Onur Vural, Maciej Kamaszewski, Deniz Ekinci
{"title":"Chronic hypoxia and hyperoxia alter tissue-specific fatty acid profile and FD6D and elongase gene expression levels in rainbow trout (Oncorhynchus mykiss).","authors":"Ercüment Aksakal, Ercan Soydan, Abdullah Tunç, Onur Vural, Maciej Kamaszewski, Deniz Ekinci","doi":"10.1007/s00360-023-01501-9","DOIUrl":"https://doi.org/10.1007/s00360-023-01501-9","url":null,"abstract":"<p><p>Commercially important trout species, especially rainbow trout, are under great threat due to several negative factors affecting oxygen levels in water such as global warming and eutrophication. In our study, rainbow trout (Oncorhynchus mykiss) was exposed to chronic (for 28 days) hypoxia (4.0 ± 0.5 mg/L) and hyperoxia (12 ± 1.2 mg/L) in order to evaluate the alteration of fatty acid profiles in muscle, liver and gill tissues. In addition, delta-6-desaturase and elongase gene expression profiles were measured in liver, kidney and gill tissues. The amount of saturated fatty acids increased by oxygen applications in the liver, while it decreased in the muscle and gill tissues compared to normoxia (p < 0.05). Monounsaturated fatty acids levels increased in muscle and gill (p < 0.05). Although n-3 polyunsaturated fatty acid (PUFA) decreased in muscle tissue, n-6 PUFA increased (p < 0.05). The n-3/n-6 ratio decreased in muscle tissue in response to the both exposures (p < 0.05) as well as eicosapentaenoic acid/docosahexaenoic acid ratio (p < 0.05). Hypoxia exposure generally increased delta-6-desaturase and elongase mRNA levels in all tissues (p < 0.05). However, gene expression profiles were variable in fish exposed to hyperoxia. As a result of oxygen exposures, the lipid profile of muscle tissue, which stores dense fat, was negatively affected more than that of liver and gill tissues. We determined that the change in expression levels was tissue specific.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":"193 4","pages":"401-412"},"PeriodicalIF":2.0,"publicationDate":"2023-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9698104","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":"Gill surface area allometry does not constrain the body mass scaling of maximum oxygen uptake rate in the tidepool sculpin, Oligocottus maculosus.","authors":"Derek A Somo, Ken Chu, Jeffrey G Richards","doi":"10.1007/s00360-023-01490-9","DOIUrl":"https://doi.org/10.1007/s00360-023-01490-9","url":null,"abstract":"<p><p>The gill oxygen limitation hypothesis (GOLH) suggests that hypometric scaling of metabolic rate in fishes is a consequence of oxygen supply constraints imposed by the mismatched growth rates of gill surface area (a two-dimensional surface) and body mass (a three-dimensional volume). GOLH may, therefore, explain the size-dependent spatial distribution of fish in temperature- and oxygen-variable environments through size-dependent respiratory capacity, but this question is unstudied. We tested GOLH in the tidepool sculpin, Oligocottus maculosus, a species in which body mass decreases with increasing temperature- and oxygen-variability in the intertidal, a pattern consistent with GOLH. We statistically evaluated support for GOLH versus distributed control of [Formula: see text] allometry by comparing scaling coefficients for gill surface area, standard and maximum [Formula: see text] ([Formula: see text]<sub>,Standard</sub> and [Formula: see text]<sub>,Max</sub>, respectively), ventricle mass, hematocrit, and metabolic enzyme activities in white muscle. To empirically evaluate whether there is a proximate constraint on oxygen supply capacity with increasing body mass, we measured [Formula: see text]<sub>,Max</sub> across a range of Po<sub>2</sub>s from normoxia to P<sub>crit</sub>, calculated the regulation value (R), a measure of oxyregulatory capacity, and analyzed the R-body mass relationship. In contrast with GOLH, gill surface area scaling either matched or was more than sufficient to meet [Formula: see text] demands with increasing body mass and R did not change with body mass. Ventricle mass (b = 1.22) scaled similarly to [Formula: see text]<sub>,Max</sub> (b = 1.18) suggesting a possible role for the heart in the scaling of [Formula: see text]<sub>,Max</sub>. Together our results do not support GOLH as a mechanism structuring the distribution of O. maculosus and suggest distributed control of oxyregulatory capacity.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":"193 4","pages":"425-438"},"PeriodicalIF":2.0,"publicationDate":"2023-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9700652","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}
Jessica M Hoffman, Britta Schmitz, Johannes U Pfabe, Sarah A Ohrnberger, Teresa G Valencak
{"title":"Lactating SKH-1 furless mice prioritize own comfort over growth of their pups.","authors":"Jessica M Hoffman, Britta Schmitz, Johannes U Pfabe, Sarah A Ohrnberger, Teresa G Valencak","doi":"10.1007/s00360-023-01498-1","DOIUrl":"10.1007/s00360-023-01498-1","url":null,"abstract":"<p><p>Lactation is the most energetically demanding physiological process that occurs in mammalian females, and as a consequence of this energy expenditure, lactating females produce an enormous amount of excess heat. This heat is thought to limit the amount of milk a mother produces, and by improving heat dissipation, females may improve their milk production and offspring quality. Here we used SKH-1 hairless mice as a natural model of improved heat dissipation. Lactating mothers were given access to a secondary cage to rest away from their pups, and this secondary cage was kept either at room temperature (22 °C) in the control rounds or cooled to 8 °C in the experimental groups. We hypothesized that the cold exposure would maximize the heat dissipation potential, leading to increased milk production and healthier pups even in the hairless mouse model. However, we found the opposite, where cold exposure allowed mothers to eat more food, but they produced smaller weight pups at the end of lactation. Our results suggest that mothers prioritize their own fitness, even if it lowers the fitness of their offspring in this particular mouse strain. This maternal-offspring trade-off is interesting and requires future studies to understand the full interaction of maternal effects and offspring fitness in the light of the heat dissipation limitation.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":"193 4","pages":"453-459"},"PeriodicalIF":1.7,"publicationDate":"2023-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10985496/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10073270","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}