Hilaire Yam Fung Cheung, Chukiat Tantiwong, Dipali Kale, Jonathan M Gibbins, Steve P Watson, Johan W M Heemskerk, Albert Sickmann, Robert Ahrends, Joanne L Dunster
{"title":"研究磷酸肌苷调控的计算框架。","authors":"Hilaire Yam Fung Cheung, Chukiat Tantiwong, Dipali Kale, Jonathan M Gibbins, Steve P Watson, Johan W M Heemskerk, Albert Sickmann, Robert Ahrends, Joanne L Dunster","doi":"10.1371/journal.pcbi.1013477","DOIUrl":null,"url":null,"abstract":"<p><p>Phosphoinositides are a group of interconvertible lipids that are located in the membrane of eukaryotic cells. They turnover via complex network of reactions (called the phosphoinositide pathway) that respond rapidly to regulate many aspects of a cell's response to their environment. Given their low-abundance they are difficult to characterise experimentally. Here we utilise a new experimental method to generate an unusually large dataset that characterises the time-dependent changes in five membrane bound phospoinositides and a soluble inositide in platelet, downstream of its GPVI receptor, where we know the phosphoinositide pathway is particularly active. To shed light on regulatotory steps that are often opaque to experimentation we use this data within a mathematical and computational framework. We construct and assess eleven mathematical models that represent competing interpretations of the dominant mechanisms that regulate the pathway. We find that while four of the models can generate the available data only one model, that incorporates an additional pool of PtdIns, is consistent with the data and is able to successfully predict the effects of an inhibitor. We publish all models openly in a form that is easily usable and adaptable for other researchers to use alongside our or their own data. We studied how changes in the shape and magnitude of events that stimulate the phosphoinositide pathway affect its dynamics. Despite these perturbations, the abundance of Phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) remained stable, consistent with findings reported in the literature.</p>","PeriodicalId":20241,"journal":{"name":"PLoS Computational Biology","volume":"21 9","pages":"e1013477"},"PeriodicalIF":3.6000,"publicationDate":"2025-09-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12510658/pdf/","citationCount":"0","resultStr":"{\"title\":\"A computational framework for the investigation of phosphoinositide regulation.\",\"authors\":\"Hilaire Yam Fung Cheung, Chukiat Tantiwong, Dipali Kale, Jonathan M Gibbins, Steve P Watson, Johan W M Heemskerk, Albert Sickmann, Robert Ahrends, Joanne L Dunster\",\"doi\":\"10.1371/journal.pcbi.1013477\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Phosphoinositides are a group of interconvertible lipids that are located in the membrane of eukaryotic cells. They turnover via complex network of reactions (called the phosphoinositide pathway) that respond rapidly to regulate many aspects of a cell's response to their environment. Given their low-abundance they are difficult to characterise experimentally. Here we utilise a new experimental method to generate an unusually large dataset that characterises the time-dependent changes in five membrane bound phospoinositides and a soluble inositide in platelet, downstream of its GPVI receptor, where we know the phosphoinositide pathway is particularly active. To shed light on regulatotory steps that are often opaque to experimentation we use this data within a mathematical and computational framework. We construct and assess eleven mathematical models that represent competing interpretations of the dominant mechanisms that regulate the pathway. We find that while four of the models can generate the available data only one model, that incorporates an additional pool of PtdIns, is consistent with the data and is able to successfully predict the effects of an inhibitor. We publish all models openly in a form that is easily usable and adaptable for other researchers to use alongside our or their own data. We studied how changes in the shape and magnitude of events that stimulate the phosphoinositide pathway affect its dynamics. Despite these perturbations, the abundance of Phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) remained stable, consistent with findings reported in the literature.</p>\",\"PeriodicalId\":20241,\"journal\":{\"name\":\"PLoS Computational Biology\",\"volume\":\"21 9\",\"pages\":\"e1013477\"},\"PeriodicalIF\":3.6000,\"publicationDate\":\"2025-09-30\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12510658/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"PLoS Computational Biology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1371/journal.pcbi.1013477\",\"RegionNum\":2,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2025/9/1 0:00:00\",\"PubModel\":\"eCollection\",\"JCR\":\"Q1\",\"JCRName\":\"BIOCHEMICAL RESEARCH METHODS\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"PLoS Computational Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1371/journal.pcbi.1013477","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/9/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"BIOCHEMICAL RESEARCH METHODS","Score":null,"Total":0}
A computational framework for the investigation of phosphoinositide regulation.
Phosphoinositides are a group of interconvertible lipids that are located in the membrane of eukaryotic cells. They turnover via complex network of reactions (called the phosphoinositide pathway) that respond rapidly to regulate many aspects of a cell's response to their environment. Given their low-abundance they are difficult to characterise experimentally. Here we utilise a new experimental method to generate an unusually large dataset that characterises the time-dependent changes in five membrane bound phospoinositides and a soluble inositide in platelet, downstream of its GPVI receptor, where we know the phosphoinositide pathway is particularly active. To shed light on regulatotory steps that are often opaque to experimentation we use this data within a mathematical and computational framework. We construct and assess eleven mathematical models that represent competing interpretations of the dominant mechanisms that regulate the pathway. We find that while four of the models can generate the available data only one model, that incorporates an additional pool of PtdIns, is consistent with the data and is able to successfully predict the effects of an inhibitor. We publish all models openly in a form that is easily usable and adaptable for other researchers to use alongside our or their own data. We studied how changes in the shape and magnitude of events that stimulate the phosphoinositide pathway affect its dynamics. Despite these perturbations, the abundance of Phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) remained stable, consistent with findings reported in the literature.
期刊介绍:
PLOS Computational Biology features works of exceptional significance that further our understanding of living systems at all scales—from molecules and cells, to patient populations and ecosystems—through the application of computational methods. Readers include life and computational scientists, who can take the important findings presented here to the next level of discovery.
Research articles must be declared as belonging to a relevant section. More information about the sections can be found in the submission guidelines.
Research articles should model aspects of biological systems, demonstrate both methodological and scientific novelty, and provide profound new biological insights.
Generally, reliability and significance of biological discovery through computation should be validated and enriched by experimental studies. Inclusion of experimental validation is not required for publication, but should be referenced where possible. Inclusion of experimental validation of a modest biological discovery through computation does not render a manuscript suitable for PLOS Computational Biology.
Research articles specifically designated as Methods papers should describe outstanding methods of exceptional importance that have been shown, or have the promise to provide new biological insights. The method must already be widely adopted, or have the promise of wide adoption by a broad community of users. Enhancements to existing published methods will only be considered if those enhancements bring exceptional new capabilities.