Pub Date : 2023-09-20eCollection Date: 2023-01-01DOI: 10.3389/fbinf.2023.1178600
David Bryant, Daniel H Huson
NeighborNet constructs phylogenetic networks to visualize distance data. It is a popular method used in a wide range of applications. While several studies have investigated its mathematical features, here we focus on computational aspects. The algorithm operates in three steps. We present a new simplified formulation of the first step, which aims at computing a circular ordering. We provide the first technical description of the second step, the estimation of split weights. We review the third step by constructing and drawing the network. Finally, we discuss how the networks might best be interpreted, review related approaches, and present some open questions.
{"title":"NeighborNet: improved algorithms and implementation.","authors":"David Bryant, Daniel H Huson","doi":"10.3389/fbinf.2023.1178600","DOIUrl":"10.3389/fbinf.2023.1178600","url":null,"abstract":"<p><p>NeighborNet constructs phylogenetic networks to visualize distance data. It is a popular method used in a wide range of applications. While several studies have investigated its mathematical features, here we focus on computational aspects. The algorithm operates in three steps. We present a new simplified formulation of the first step, which aims at computing a circular ordering. We provide the first technical description of the second step, the estimation of split weights. We review the third step by constructing and drawing the network. Finally, we discuss how the networks might best be interpreted, review related approaches, and present some open questions.</p>","PeriodicalId":73066,"journal":{"name":"Frontiers in bioinformatics","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2023-09-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10548196/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41161536","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-09-19eCollection Date: 2023-01-01DOI: 10.3389/fbinf.2023.1248732
Niloofar Shirvanizadeh, Mauno Vihinen
{"title":"VariBench, new variation benchmark categories and data sets.","authors":"Niloofar Shirvanizadeh, Mauno Vihinen","doi":"10.3389/fbinf.2023.1248732","DOIUrl":"10.3389/fbinf.2023.1248732","url":null,"abstract":"","PeriodicalId":73066,"journal":{"name":"Frontiers in bioinformatics","volume":null,"pages":null},"PeriodicalIF":2.8,"publicationDate":"2023-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10546188/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41167306","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-09-13eCollection Date: 2023-01-01DOI: 10.3389/fbinf.2023.1287407
Mohammed Zidane, Ahmad Makky, Matthias Bruhns, Alexander Rochwarger, Sepideh Babaei, Manfred Claassen, Christian M Schürch
[This corrects the article DOI: 10.3389/fbinf.2023.1159381.].
[这更正了文章DOI:10.3389/fbinf.2023.1159381.]。
{"title":"Corrigendum: A review on deep learning applications in highly multiplexed tissue imaging data analysis.","authors":"Mohammed Zidane, Ahmad Makky, Matthias Bruhns, Alexander Rochwarger, Sepideh Babaei, Manfred Claassen, Christian M Schürch","doi":"10.3389/fbinf.2023.1287407","DOIUrl":"10.3389/fbinf.2023.1287407","url":null,"abstract":"<p><p>[This corrects the article DOI: 10.3389/fbinf.2023.1159381.].</p>","PeriodicalId":73066,"journal":{"name":"Frontiers in bioinformatics","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2023-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10534973/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41170250","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Peptide informatics is a rapidly growing field that is at the intersection of bioinformatics, chemistry, and biology. Peptides are short chains of amino acids that play important roles in a wide variety of biological processes, such as protein folding, signal transduction, and immune function. Peptide informatics is the use of computational methods to study peptides and their sequence, structure, function, and interactions. Recent advances in peptide informatics have led to a number of new discoveries and applications. For example, new methods have been developed to predict the structure of peptides, which can be used to design new drugs and therapies. New methods for identifying peptide-protein interactions have also been introduced, which can be used to understand the molecular basis of disease.
{"title":"Editorial: Recent advances in peptide informatics: challenges and opportunities.","authors":"Rahul Kumar, Kumardeep Chaudhary, Sandeep Kumar Dhanda","doi":"10.3389/fbinf.2023.1271932","DOIUrl":"https://doi.org/10.3389/fbinf.2023.1271932","url":null,"abstract":"Peptide informatics is a rapidly growing field that is at the intersection of bioinformatics, chemistry, and biology. Peptides are short chains of amino acids that play important roles in a wide variety of biological processes, such as protein folding, signal transduction, and immune function. Peptide informatics is the use of computational methods to study peptides and their sequence, structure, function, and interactions. Recent advances in peptide informatics have led to a number of new discoveries and applications. For example, new methods have been developed to predict the structure of peptides, which can be used to design new drugs and therapies. New methods for identifying peptide-protein interactions have also been introduced, which can be used to understand the molecular basis of disease.","PeriodicalId":73066,"journal":{"name":"Frontiers in bioinformatics","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2023-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10523389/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41155909","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-09-01eCollection Date: 2023-01-01DOI: 10.3389/fbinf.2023.1233281
Jack M Craig, Sudhir Kumar, S Blair Hedges
The origin of eukaryotes was among the most important events in the history of life, spawning a new evolutionary lineage that led to all complex multicellular organisms. However, the timing of this event, crucial for understanding its environmental context, has been difficult to establish. The fossil and biomarker records are sparse and molecular clocks have thus far not reached a consensus, with dates spanning 2.1-0.91 billion years ago (Ga) for critical nodes. Notably, molecular time estimates for the last common ancestor of eukaryotes are typically hundreds of millions of years younger than the Great Oxidation Event (GOE, 2.43-2.22 Ga), leading researchers to question the presumptive link between eukaryotes and oxygen. We obtained a new time estimate for the origin of eukaryotes using genetic data of both archaeal and bacterial origin, the latter rarely used in past studies. We also avoided potential calibration biases that may have affected earlier studies. We obtained a conservative interval of 2.2-1.5 Ga, with an even narrower core interval of 2.0-1.8 Ga, for the origin of eukaryotes, a period closely aligned with the rise in oxygen. We further reconstructed the history of biological complexity across the tree of life using three universal measures: cell types, genes, and genome size. We found that the rise in complexity was temporally consistent with and followed a pattern similar to the rise in oxygen. This suggests a causal relationship stemming from the increased energy needs of complex life fulfilled by oxygen.
{"title":"The origin of eukaryotes and rise in complexity were synchronous with the rise in oxygen.","authors":"Jack M Craig, Sudhir Kumar, S Blair Hedges","doi":"10.3389/fbinf.2023.1233281","DOIUrl":"10.3389/fbinf.2023.1233281","url":null,"abstract":"<p><p>The origin of eukaryotes was among the most important events in the history of life, spawning a new evolutionary lineage that led to all complex multicellular organisms. However, the timing of this event, crucial for understanding its environmental context, has been difficult to establish. The fossil and biomarker records are sparse and molecular clocks have thus far not reached a consensus, with dates spanning 2.1-0.91 billion years ago (Ga) for critical nodes. Notably, molecular time estimates for the last common ancestor of eukaryotes are typically hundreds of millions of years younger than the Great Oxidation Event (GOE, 2.43-2.22 Ga), leading researchers to question the presumptive link between eukaryotes and oxygen. We obtained a new time estimate for the origin of eukaryotes using genetic data of both archaeal and bacterial origin, the latter rarely used in past studies. We also avoided potential calibration biases that may have affected earlier studies. We obtained a conservative interval of 2.2-1.5 Ga, with an even narrower core interval of 2.0-1.8 Ga, for the origin of eukaryotes, a period closely aligned with the rise in oxygen. We further reconstructed the history of biological complexity across the tree of life using three universal measures: cell types, genes, and genome size. We found that the rise in complexity was temporally consistent with and followed a pattern similar to the rise in oxygen. This suggests a causal relationship stemming from the increased energy needs of complex life fulfilled by oxygen.</p>","PeriodicalId":73066,"journal":{"name":"Frontiers in bioinformatics","volume":null,"pages":null},"PeriodicalIF":2.8,"publicationDate":"2023-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10505794/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41142624","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Conventional dimensionality reduction methods like Multidimensional Scaling (MDS) are sensitive to the presence of orthogonal outliers, leading to significant defects in the embedding. We introduce a robust MDS method, called DeCOr-MDS (Detection and Correction of Orthogonal outliers using MDS), based on the geometry and statistics of simplices formed by data points, that allows to detect orthogonal outliers and subsequently reduce dimensionality. We validate our methods using synthetic datasets, and further show how it can be applied to a variety of large real biological datasets, including cancer image cell data, human microbiome project data and single cell RNA sequencing data, to address the task of data cleaning and visualization.
{"title":"Orthogonal outlier detection and dimension estimation for improved MDS embedding of biological datasets.","authors":"Wanxin Li, Jules Mirone, Ashok Prasad, Nina Miolane, Carine Legrand, Khanh Dao Duc","doi":"10.3389/fbinf.2023.1211819","DOIUrl":"10.3389/fbinf.2023.1211819","url":null,"abstract":"<p><p>Conventional dimensionality reduction methods like Multidimensional Scaling (MDS) are sensitive to the presence of orthogonal outliers, leading to significant defects in the embedding. We introduce a robust MDS method, called <i>DeCOr-MDS</i> (Detection and Correction of Orthogonal outliers using MDS), based on the geometry and statistics of simplices formed by data points, that allows to detect orthogonal outliers and subsequently reduce dimensionality. We validate our methods using synthetic datasets, and further show how it can be applied to a variety of large real biological datasets, including cancer image cell data, human microbiome project data and single cell RNA sequencing data, to address the task of data cleaning and visualization.</p>","PeriodicalId":73066,"journal":{"name":"Frontiers in bioinformatics","volume":null,"pages":null},"PeriodicalIF":2.8,"publicationDate":"2023-08-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10448701/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10100807","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-08-03eCollection Date: 2023-01-01DOI: 10.3389/fbinf.2023.1225807
Jose Barba-Montoya, Sudip Sharma, Sudhir Kumar
A common practice in molecular systematics is to infer phylogeny and then scale it to time by using a relaxed clock method and calibrations. This sequential analysis practice ignores the effect of phylogenetic uncertainty on divergence time estimates and their confidence/credibility intervals. An alternative is to infer phylogeny and times jointly to incorporate phylogenetic errors into molecular dating. We compared the performance of these two alternatives in reconstructing evolutionary timetrees using computer-simulated and empirical datasets. We found sequential and joint analyses to produce similar divergence times and phylogenetic relationships, except for some nodes in particular cases. The joint inference performed better when the phylogeny was not well resolved, situations in which the joint inference should be preferred. However, joint inference can be infeasible for large datasets because available Bayesian methods are computationally burdensome. We present an alternative approach for joint inference that combines the bag of little bootstraps, maximum likelihood, and RelTime approaches for simultaneously inferring evolutionary relationships, divergence times, and confidence intervals, incorporating phylogeny uncertainty. The new method alleviates the high computational burden imposed by Bayesian methods while achieving a similar result.
{"title":"Molecular timetrees using relaxed clocks and uncertain phylogenies.","authors":"Jose Barba-Montoya, Sudip Sharma, Sudhir Kumar","doi":"10.3389/fbinf.2023.1225807","DOIUrl":"10.3389/fbinf.2023.1225807","url":null,"abstract":"<p><p>A common practice in molecular systematics is to infer phylogeny and then scale it to time by using a relaxed clock method and calibrations. This sequential analysis practice ignores the effect of phylogenetic uncertainty on divergence time estimates and their confidence/credibility intervals. An alternative is to infer phylogeny and times jointly to incorporate phylogenetic errors into molecular dating. We compared the performance of these two alternatives in reconstructing evolutionary timetrees using computer-simulated and empirical datasets. We found sequential and joint analyses to produce similar divergence times and phylogenetic relationships, except for some nodes in particular cases. The joint inference performed better when the phylogeny was not well resolved, situations in which the joint inference should be preferred. However, joint inference can be infeasible for large datasets because available Bayesian methods are computationally burdensome. We present an alternative approach for joint inference that combines the bag of little bootstraps, maximum likelihood, and RelTime approaches for simultaneously inferring evolutionary relationships, divergence times, and confidence intervals, incorporating phylogeny uncertainty. The new method alleviates the high computational burden imposed by Bayesian methods while achieving a similar result.</p>","PeriodicalId":73066,"journal":{"name":"Frontiers in bioinformatics","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2023-08-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10435864/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10046632","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-08-02eCollection Date: 2023-01-01DOI: 10.3389/fbinf.2023.1164482
Zihao Wang, Yun Zhou, Yu Zhang, Yu K Mo, Yijie Wang
Introduction: Existing large-scale preclinical cancer drug response databases provide us with a great opportunity to identify and predict potentially effective drugs to combat cancers. Deep learning models built on these databases have been developed and applied to tackle the cancer drug-response prediction task. Their prediction has been demonstrated to significantly outperform traditional machine learning methods. However, due to the "black box" characteristic, biologically faithful explanations are hardly derived from these deep learning models. Interpretable deep learning models that rely on visible neural networks (VNNs) have been proposed to provide biological justification for the predicted outcomes. However, their performance does not meet the expectation to be applied in clinical practice. Methods: In this paper, we develop an XMR model, an eXplainable Multimodal neural network for drug Response prediction. XMR is a new compact multimodal neural network consisting of two sub-networks: a visible neural network for learning genomic features and a graph neural network (GNN) for learning drugs' structural features. Both sub-networks are integrated into a multimodal fusion layer to model the drug response for the given gene mutations and the drug's molecular structures. Furthermore, a pruning approach is applied to provide better interpretations of the XMR model. We use five pathway hierarchies (cell cycle, DNA repair, diseases, signal transduction, and metabolism), which are obtained from the Reactome Pathway Database, as the architecture of VNN for our XMR model to predict drug responses of triple negative breast cancer. Results: We find that our model outperforms other state-of-the-art interpretable deep learning models in terms of predictive performance. In addition, our model can provide biological insights into explaining drug responses for triple-negative breast cancer. Discussion: Overall, combining both VNN and GNN in a multimodal fusion layer, XMR captures key genomic and molecular features and offers reasonable interpretability in biology, thereby better predicting drug responses in cancer patients. Our model would also benefit personalized cancer therapy in the future.
{"title":"XMR: an explainable multimodal neural network for drug response prediction.","authors":"Zihao Wang, Yun Zhou, Yu Zhang, Yu K Mo, Yijie Wang","doi":"10.3389/fbinf.2023.1164482","DOIUrl":"10.3389/fbinf.2023.1164482","url":null,"abstract":"<p><p><b>Introduction:</b> Existing large-scale preclinical cancer drug response databases provide us with a great opportunity to identify and predict potentially effective drugs to combat cancers. Deep learning models built on these databases have been developed and applied to tackle the cancer drug-response prediction task. Their prediction has been demonstrated to significantly outperform traditional machine learning methods. However, due to the \"black box\" characteristic, biologically faithful explanations are hardly derived from these deep learning models. Interpretable deep learning models that rely on visible neural networks (VNNs) have been proposed to provide biological justification for the predicted outcomes. However, their performance does not meet the expectation to be applied in clinical practice. <b>Methods:</b> In this paper, we develop an XMR model, an eXplainable Multimodal neural network for drug Response prediction. XMR is a new compact multimodal neural network consisting of two sub-networks: a visible neural network for learning genomic features and a graph neural network (GNN) for learning drugs' structural features. Both sub-networks are integrated into a multimodal fusion layer to model the drug response for the given gene mutations and the drug's molecular structures. Furthermore, a pruning approach is applied to provide better interpretations of the XMR model. We use five pathway hierarchies (cell cycle, DNA repair, diseases, signal transduction, and metabolism), which are obtained from the Reactome Pathway Database, as the architecture of VNN for our XMR model to predict drug responses of triple negative breast cancer. <b>Results:</b> We find that our model outperforms other state-of-the-art interpretable deep learning models in terms of predictive performance. In addition, our model can provide biological insights into explaining drug responses for triple-negative breast cancer. <b>Discussion:</b> Overall, combining both VNN and GNN in a multimodal fusion layer, XMR captures key genomic and molecular features and offers reasonable interpretability in biology, thereby better predicting drug responses in cancer patients. Our model would also benefit personalized cancer therapy in the future.</p>","PeriodicalId":73066,"journal":{"name":"Frontiers in bioinformatics","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2023-08-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10433751/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10039829","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-07-27eCollection Date: 2023-01-01DOI: 10.3389/fbinf.2023.1234218
Ryan S McClure, Yvonne Rericha, Katrina M Waters, Robyn L Tanguay
Introduction: The application of RNA-sequencing has led to numerous breakthroughs related to investigating gene expression levels in complex biological systems. Among these are knowledge of how organisms, such as the vertebrate model organism zebrafish (Danio rerio), respond to toxicant exposure. Recently, the development of 3' RNA-seq has allowed for the determination of gene expression levels with a fraction of the required reads compared to standard RNA-seq. While 3' RNA-seq has many advantages, a comparison to standard RNA-seq has not been performed in the context of whole organism toxicity and sparse data. Methods and results: Here, we examined samples from zebrafish exposed to perfluorobutane sulfonamide (FBSA) with either 3' or standard RNA-seq to determine the advantages of each with regards to the identification of functionally enriched pathways. We found that 3' and standard RNA-seq showed specific advantages when focusing on annotated or unannotated regions of the genome. We also found that standard RNA-seq identified more differentially expressed genes (DEGs), but that this advantage disappeared under conditions of sparse data. We also found that standard RNA-seq had a significant advantage in identifying functionally enriched pathways via analysis of DEG lists but that this advantage was minimal when identifying pathways via gene set enrichment analysis of all genes. Conclusions: These results show that each approach has experimental conditions where they may be advantageous. Our observations can help guide others in the choice of 3' RNA-seq vs standard RNA sequencing to query gene expression levels in a range of biological systems.
{"title":"3' RNA-seq is superior to standard RNA-seq in cases of sparse data but inferior at identifying toxicity pathways in a model organism.","authors":"Ryan S McClure, Yvonne Rericha, Katrina M Waters, Robyn L Tanguay","doi":"10.3389/fbinf.2023.1234218","DOIUrl":"10.3389/fbinf.2023.1234218","url":null,"abstract":"<p><p><b>Introduction:</b> The application of RNA-sequencing has led to numerous breakthroughs related to investigating gene expression levels in complex biological systems. Among these are knowledge of how organisms, such as the vertebrate model organism zebrafish (<i>Danio rerio</i>), respond to toxicant exposure. Recently, the development of 3' RNA-seq has allowed for the determination of gene expression levels with a fraction of the required reads compared to standard RNA-seq. While 3' RNA-seq has many advantages, a comparison to standard RNA-seq has not been performed in the context of whole organism toxicity and sparse data. <b>Methods and results:</b> Here, we examined samples from zebrafish exposed to perfluorobutane sulfonamide (FBSA) with either 3' or standard RNA-seq to determine the advantages of each with regards to the identification of functionally enriched pathways. We found that 3' and standard RNA-seq showed specific advantages when focusing on annotated or unannotated regions of the genome. We also found that standard RNA-seq identified more differentially expressed genes (DEGs), but that this advantage disappeared under conditions of sparse data. We also found that standard RNA-seq had a significant advantage in identifying functionally enriched pathways via analysis of DEG lists but that this advantage was minimal when identifying pathways via gene set enrichment analysis of all genes. <b>Conclusions:</b> These results show that each approach has experimental conditions where they may be advantageous. Our observations can help guide others in the choice of 3' RNA-seq vs standard RNA sequencing to query gene expression levels in a range of biological systems.</p>","PeriodicalId":73066,"journal":{"name":"Frontiers in bioinformatics","volume":null,"pages":null},"PeriodicalIF":2.8,"publicationDate":"2023-07-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10414111/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9990456","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}