Robert E Kwait, Evan A Eskew, Malin L Pinsky, Sarah A Gignoux-Wolfsohn, Maarten J Vonhof, Brooke Maslo
{"title":"暴露于白鼻综合征的小棕蝠的细胞因子风暴和败血症的转录组学证据。","authors":"Robert E Kwait, Evan A Eskew, Malin L Pinsky, Sarah A Gignoux-Wolfsohn, Maarten J Vonhof, Brooke Maslo","doi":"10.1093/conphys/coaf040","DOIUrl":null,"url":null,"abstract":"<p><p>Much progress has been made in understanding the pathophysiology of white-nose syndrome (WNS), a devastating disease that has impacted North American hibernating bats for nearly two decades. Growth of the causative fungal pathogen, <i>Pseudogymnoascus destructans,</i> on exposed epidermal tissue of bats creates an immune reaction that disrupts natural hibernation physiology and leads to premature expenditure of energy reserves and often death. Past work has highlighted the similarities between WNS and immune reconstitution inflammatory syndrome, but other conditions that have not been considered yet may also be relevant. We performed a transcriptomic analysis of wing tissue from naïve and exposed bats to further investigate the implications of observed differential gene expression patterns. For this analysis, we collected wing biopsy samples from 41 individuals prior to WNS emergence and 58 individuals 2-5 years after WNS emergence. We generated poly-A enriched tag-Seq libraries to compare gene expression between these groups. We then linked our findings and those of past studies to other disease systems to build hypotheses regarding mechanisms of WNS pathophysiology. We found an overrepresentation of functions related to programmed cell death and cytokine activity among upregulated genes. Importantly, we also identified upregulation of three S100 damage-associated molecular patterns (DAMPs) in exposed populations. Taken together, our findings and those of past studies suggest that infected bats experience a feedback loop of cell death among immune cells, the release of DAMPs and the stimulation of cytokine release that may act to maintain pathological immune activity. This feedback loop likely relates to cytokine storms in individuals with severe infection and possibly deteriorates into sepsis over time. Given the pathophysiology of sepsis, multiple organ dysfunction potentially contributes to the physiological disruption associated with WNS.</p>","PeriodicalId":54331,"journal":{"name":"Conservation Physiology","volume":"13 1","pages":"coaf040"},"PeriodicalIF":2.5000,"publicationDate":"2025-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12212055/pdf/","citationCount":"0","resultStr":"{\"title\":\"Transcriptomic evidence of cytokine storm and sepsis in little brown bats exposed to white-nose syndrome.\",\"authors\":\"Robert E Kwait, Evan A Eskew, Malin L Pinsky, Sarah A Gignoux-Wolfsohn, Maarten J Vonhof, Brooke Maslo\",\"doi\":\"10.1093/conphys/coaf040\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Much progress has been made in understanding the pathophysiology of white-nose syndrome (WNS), a devastating disease that has impacted North American hibernating bats for nearly two decades. Growth of the causative fungal pathogen, <i>Pseudogymnoascus destructans,</i> on exposed epidermal tissue of bats creates an immune reaction that disrupts natural hibernation physiology and leads to premature expenditure of energy reserves and often death. Past work has highlighted the similarities between WNS and immune reconstitution inflammatory syndrome, but other conditions that have not been considered yet may also be relevant. We performed a transcriptomic analysis of wing tissue from naïve and exposed bats to further investigate the implications of observed differential gene expression patterns. For this analysis, we collected wing biopsy samples from 41 individuals prior to WNS emergence and 58 individuals 2-5 years after WNS emergence. We generated poly-A enriched tag-Seq libraries to compare gene expression between these groups. We then linked our findings and those of past studies to other disease systems to build hypotheses regarding mechanisms of WNS pathophysiology. We found an overrepresentation of functions related to programmed cell death and cytokine activity among upregulated genes. Importantly, we also identified upregulation of three S100 damage-associated molecular patterns (DAMPs) in exposed populations. Taken together, our findings and those of past studies suggest that infected bats experience a feedback loop of cell death among immune cells, the release of DAMPs and the stimulation of cytokine release that may act to maintain pathological immune activity. This feedback loop likely relates to cytokine storms in individuals with severe infection and possibly deteriorates into sepsis over time. Given the pathophysiology of sepsis, multiple organ dysfunction potentially contributes to the physiological disruption associated with WNS.</p>\",\"PeriodicalId\":54331,\"journal\":{\"name\":\"Conservation Physiology\",\"volume\":\"13 1\",\"pages\":\"coaf040\"},\"PeriodicalIF\":2.5000,\"publicationDate\":\"2025-07-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12212055/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Conservation Physiology\",\"FirstCategoryId\":\"93\",\"ListUrlMain\":\"https://doi.org/10.1093/conphys/coaf040\",\"RegionNum\":3,\"RegionCategory\":\"环境科学与生态学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2025/1/1 0:00:00\",\"PubModel\":\"eCollection\",\"JCR\":\"Q2\",\"JCRName\":\"BIODIVERSITY CONSERVATION\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Conservation Physiology","FirstCategoryId":"93","ListUrlMain":"https://doi.org/10.1093/conphys/coaf040","RegionNum":3,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/1/1 0:00:00","PubModel":"eCollection","JCR":"Q2","JCRName":"BIODIVERSITY CONSERVATION","Score":null,"Total":0}
Transcriptomic evidence of cytokine storm and sepsis in little brown bats exposed to white-nose syndrome.
Much progress has been made in understanding the pathophysiology of white-nose syndrome (WNS), a devastating disease that has impacted North American hibernating bats for nearly two decades. Growth of the causative fungal pathogen, Pseudogymnoascus destructans, on exposed epidermal tissue of bats creates an immune reaction that disrupts natural hibernation physiology and leads to premature expenditure of energy reserves and often death. Past work has highlighted the similarities between WNS and immune reconstitution inflammatory syndrome, but other conditions that have not been considered yet may also be relevant. We performed a transcriptomic analysis of wing tissue from naïve and exposed bats to further investigate the implications of observed differential gene expression patterns. For this analysis, we collected wing biopsy samples from 41 individuals prior to WNS emergence and 58 individuals 2-5 years after WNS emergence. We generated poly-A enriched tag-Seq libraries to compare gene expression between these groups. We then linked our findings and those of past studies to other disease systems to build hypotheses regarding mechanisms of WNS pathophysiology. We found an overrepresentation of functions related to programmed cell death and cytokine activity among upregulated genes. Importantly, we also identified upregulation of three S100 damage-associated molecular patterns (DAMPs) in exposed populations. Taken together, our findings and those of past studies suggest that infected bats experience a feedback loop of cell death among immune cells, the release of DAMPs and the stimulation of cytokine release that may act to maintain pathological immune activity. This feedback loop likely relates to cytokine storms in individuals with severe infection and possibly deteriorates into sepsis over time. Given the pathophysiology of sepsis, multiple organ dysfunction potentially contributes to the physiological disruption associated with WNS.
期刊介绍:
Conservation Physiology is an online only, fully open access journal published on behalf of the Society for Experimental Biology.
Biodiversity across the globe faces a growing number of threats associated with human activities. Conservation Physiology will publish research on all taxa (microbes, plants and animals) focused on understanding and predicting how organisms, populations, ecosystems and natural resources respond to environmental change and stressors. Physiology is considered in the broadest possible terms to include functional and mechanistic responses at all scales. We also welcome research towards developing and refining strategies to rebuild populations, restore ecosystems, inform conservation policy, and manage living resources. We define conservation physiology broadly and encourage potential authors to contact the editorial team if they have any questions regarding the remit of the journal.