{"title":"Comparison of <i>N-</i> and <i>O-</i>Glycosylation on Spike Glycoprotein 1 of SARS-CoV-1 and MERS-CoV.","authors":"Yuan Tian, John F Cipollo","doi":"10.1021/acs.jproteome.4c00716","DOIUrl":"10.1021/acs.jproteome.4c00716","url":null,"abstract":"<p><p>SARS-CoV-1 and MERS-CoV were the infective agents of the 2002 and 2012 coronavirus outbreaks, respectively. Here, we report a comparative liquid chromatography/mass spectrometry (LC/MS) Orbitrap <i>N-</i> and <i>O-</i>glycosylation glycoproteomics study of the recombinant S1 spike derived from these two viruses. The former was produced in HEK293 cells and the latter in both HEK293 and insect cells. Both proteins were highly glycosylated, with SARS-CoV-1 S1 having 13 and MERS-CoV S1 having 12 <i>N-</i>glycosites. Nearly all were occupied at 85% or more. Between 2 and 113 unique <i>N-</i>glycan compositions were detected at each <i>N-</i>glycosite across the three proteins. Complex <i>N</i>-glycans dominated in HEK293 cell-derived spike S1 proteins. While glycosylation differs between HEK293 and insect cells, the extent of glycan processing at glycosites was similar for the two MERS-CoV S1 forms. The HEK293-derived SARS-CoV-1 S1 <i>N-</i>glycans were more highly sialylated and fucosylated compared to MERS S1, while the latter had more high-mannose glycosides, particularly in the <i>N</i>-terminus and near the RBD. Seven and 8 <i>O</i>-glycosites were identified in SARS-CoV-1 S1 and MERS-CoV S1, respectively. Mapping of predicted antigenic and glycosylation sites reveals colocalization consistent with a role for glycosylation in immune system avoidance. Glycosylation patterns of these S1 proteins differ from those of other SARS-CoV-1 and MERS-CoV spike reported forms such as recombinant trimeric and virus-propagated forms, which has implications for virus research, including vaccine development, as glycosylation plays a role in spike function and epitope structure.</p>","PeriodicalId":48,"journal":{"name":"Journal of Proteome Research","volume":" ","pages":"2256-2265"},"PeriodicalIF":3.8,"publicationDate":"2025-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143802035","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Journal of Proteome ResearchPub Date : 2025-05-02DOI: 10.1021/acs.jproteome.5c0035210.1021/acs.jproteome.5c00352
John R. Yates III, Claire E. Eyers, Magnus Palmblad, Thomas Kislinger, Elaine Holmes, Jennifer Geddes-McAlister, Suman S. Thakur, Ryan T. Kelly, Huilin Li and Uwe Völker,
{"title":"Proteomic and Metabolomic Data Transparency","authors":"John R. Yates III, Claire E. Eyers, Magnus Palmblad, Thomas Kislinger, Elaine Holmes, Jennifer Geddes-McAlister, Suman S. Thakur, Ryan T. Kelly, Huilin Li and Uwe Völker, ","doi":"10.1021/acs.jproteome.5c0035210.1021/acs.jproteome.5c00352","DOIUrl":"https://doi.org/10.1021/acs.jproteome.5c00352https://doi.org/10.1021/acs.jproteome.5c00352","url":null,"abstract":"","PeriodicalId":48,"journal":{"name":"Journal of Proteome Research","volume":"24 5","pages":"2207 2207"},"PeriodicalIF":3.8,"publicationDate":"2025-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143894081","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Isabel Gimeno, María Berdasco, Miguel L Pato, Pascal Salvetti, Susana Carrocera, Aurora García, Enrique Gómez
{"title":"Calf Fitness Associates with Early Embryo and Recipient Metabolomes and with Calf Epigenetic Marks.","authors":"Isabel Gimeno, María Berdasco, Miguel L Pato, Pascal Salvetti, Susana Carrocera, Aurora García, Enrique Gómez","doi":"10.1021/acs.jproteome.4c00987","DOIUrl":"https://doi.org/10.1021/acs.jproteome.4c00987","url":null,"abstract":"<p><p>We used metadata to explore the metabolic interplay between culture medium from in vitro-produced bovine embryos transferred fresh or frozen, recipient blood plasma, and calf fitness, alongside gene expression and methylation in calf lymphocytes. Principal component (PC) analysis (PCA) identified covariates that were depicted in Debiased Sparse Partial Correlation networks and analyzed as enriched pathways. Four PCs explained 13.77, 9.58, 7.73 and 5.84% variability. PC1 clustered only mother weight and two embryonic metabolites. PC2, PC3 and PC4 associated 10, 17, and 5 calf features with 10, 6, and 16 embryonic and 2, 20, and 5 recipient metabolites, respectively. Subsequently, gene methylation and expression, and calf fitness were analyzed by PCA. Three PCs covered 100% variability. PC1 associated acid-base balance, protein metabolism, Cl<sup>-</sup>, and Ca<sup>2+</sup> with <i>IGF2</i> and <i>IL1R1</i> expression, and <i>IL4</i> and <i>IL12B</i> methylation. PC2 linked <i>H19</i> expression and methylation with growth and biochemical traits. PC3 clustered growth, hydration, and redox balance, with <i>IGF2</i>, <i>IGF2R</i>, <i>IL1R1</i> and <i>IL3</i> methylation, and <i>H19</i>, <i>IGF2</i>, <i>IGF2R</i> and <i>IL12B</i> expression. Gene methylation connected with embryo metabolites through networks via K<sup>+</sup>, Cl<sup>-</sup>, HCO<sub>3</sub><sup>-</sup> and TCO<sub>2</sub>. Calf fitness parallels the early metabolic fingerprints of the embryo and recipient, allowing embryo transfer decision-making based on calf health.</p>","PeriodicalId":48,"journal":{"name":"Journal of Proteome Research","volume":"24 5","pages":"2386-2402"},"PeriodicalIF":3.8,"publicationDate":"2025-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143952109","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Apostolos Gkantzos, Stavros Kalogiannis, Olga Deda
{"title":"The Role of Aromatic Amino Acids in Polycystic Ovary Syndrome through Patients' Blood Metabolic Profiling: A Systematic Review of the Past Five Years.","authors":"Apostolos Gkantzos, Stavros Kalogiannis, Olga Deda","doi":"10.1021/acs.jproteome.4c00937","DOIUrl":"https://doi.org/10.1021/acs.jproteome.4c00937","url":null,"abstract":"<p><p>Polycystic ovary syndrome (PCOS) is a common endocrine and metabolic disorder in women of reproductive age that encompasses a multitude of signs and symptoms, including hyperandrogenism, polycystic ovarian morphology, ovulatory dysfunction, and insulin resistance. The study aims to explore the role of aromatic amino acid (AAA) disorders in the syndrome. A systematic search on the databases Scopus, PubMed, and Google Scholar until 20 July 2024 over the past 5 years regarding metabolomic studies on PCOS patients' blood and the status of AAAs resulted in 12 related papers. Our review showed that AAA metabolic pathways are dysregulated, and their levels in the blood serum and plasma of PCOS patients in most studies are elevated due to inflammation and oxidative stress which, assisted by gut dysbiosis, give rise to insulin resistance that develops into PCOS. AAA abnormalities can also directly induce the defining symptoms of the syndrome through diminished neurotransmitter availability and impaired signaling. According to our review, AAA perturbations are detected in every stage of PCOS pathophysiology, making them valuable biomarkers for early diagnosis and management of the syndrome. Further investigation of the biological function, role, and impact of AAAs, probably alongside other metabolites, including BCAAs, could lead to the discovery of new tools for preventing and managing PCOS symptoms.</p>","PeriodicalId":48,"journal":{"name":"Journal of Proteome Research","volume":"24 5","pages":"2208-2221"},"PeriodicalIF":3.8,"publicationDate":"2025-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12053951/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143951604","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Hassan Hijazi, Julie Manessier, Sabine Brugiere, Tina Ravnsborg, Marie Courçon, Baptiste Brule, Karine Merienne, Ole N Jensen, Anne-Marie Hesse, Christophe Bruley, Delphine Pflieger
{"title":"Mind Your Spectra: Points to be Aware of When Validating the Identification of Isobaric Histone Peptidoforms.","authors":"Hassan Hijazi, Julie Manessier, Sabine Brugiere, Tina Ravnsborg, Marie Courçon, Baptiste Brule, Karine Merienne, Ole N Jensen, Anne-Marie Hesse, Christophe Bruley, Delphine Pflieger","doi":"10.1021/acs.jproteome.4c01056","DOIUrl":"10.1021/acs.jproteome.4c01056","url":null,"abstract":"<p><p>Mass spectrometry has become central to identifying and quantifying histone post-translational modifications (PTMs), surpassing limitations of antibody-based methods. Histones are dynamically modified by multiple structures, especially at lysine residues on their N-terminal tails, to regulate DNA-templated processes. Reliable identification of histone PTMs remains challenging and still requires manual curation. This study focused on the Lys27-Arg40 stretch of histone H3, considered four sequence variants, an increasing number of lysine PTMs and artifacts coming from histone sample processing, which resulted in many isobaric peptides. Our analysis revealed the value of low-mass b1 and cyclic immonium fragment ions to validate identification of the distinct peptidoforms. We examined how MS/MS spectra are transformed by common identification software during the conversion of raw files into peak lists, and highlighted how some parameters may erase the informative low-mass fragments. We targeted the detection of 40 H3 K27-R40 variant × PTM combinations, including the mouse-specific variants H3mm7 and H3mm13, in histone samples extracted from mouse testis and brain via a parallel reaction monitoring analysis. We only detected very low levels of unmodified H3mm7. Our work contributes to reliably deciphering the histone code shaped by distinct sequence variants and numerous combinations of PTMs.</p>","PeriodicalId":48,"journal":{"name":"Journal of Proteome Research","volume":" ","pages":"2408-2418"},"PeriodicalIF":3.8,"publicationDate":"2025-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143750277","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Carlyn M Guthrie, Amber C Meeker, Ashton E Self, Aidaly Ramos-Leyva, Olivia L Clark, Stephen K Kotey, Steven D Hartson, Yurong Liang, Lin Liu, Xuejuan Tan, Yong Cheng
{"title":"Microvesicles Derived from Human Bronchial Epithelial Cells Regulate Macrophage Activation During <i>Mycobacterium abscessus</i> Infection.","authors":"Carlyn M Guthrie, Amber C Meeker, Ashton E Self, Aidaly Ramos-Leyva, Olivia L Clark, Stephen K Kotey, Steven D Hartson, Yurong Liang, Lin Liu, Xuejuan Tan, Yong Cheng","doi":"10.1021/acs.jproteome.4c00827","DOIUrl":"10.1021/acs.jproteome.4c00827","url":null,"abstract":"<p><p>Intercellular communication is important for host immunity in response to bacterial infections. Nontuberculous mycobacterium (NTM), such as <i>Mycobacterium abscessus</i> (<i>M. ab</i>), is a group of environmental bacteria that can cause severe lung infections in individuals with pre-existing lung conditions, including cystic fibrosis (CF) and chronic obstructive pulmonary disease (COPD). There is limited knowledge understanding the interaction between airway epithelial cells and immune cells during NTM infections. In this study, we characterized microvesicles (MVs) released from uninfected and <i>M. ab</i>-infected human bronchial epithelial cells and investigated the effect of these MVs on the activation and polarization of THP-1-derived macrophages in cell culture. Our results indicate that MVs released by <i>M. ab</i>-infected human bronchial epithelial cells stimulated the activation of M2-polarized macrophages in cell culture when compared to MVs released by uninfected cells. Additionally, the proteomic analysis for isolated MVs showed that the proteins involved in the cell adhesion pathway were enriched in MVs from <i>M. ab</i>-infected human bronchial epithelial cells compared to MVs from uninfected cells. Among those, the cell surface protein, intercellular adhesion molecule 1 (ICAM-1), regulated the uptake of MVs released by <i>M. ab</i>-infected human bronchial epithelial cells by recipient macrophages in cell culture. In conclusion, our data suggest that in response to <i>M. ab</i> infection, human airway epithelial cells release MVs to modulate the activation of macrophages, which are key cells for mycobacterial intracellular survival in the host.</p>","PeriodicalId":48,"journal":{"name":"Journal of Proteome Research","volume":" ","pages":"2291-2301"},"PeriodicalIF":3.8,"publicationDate":"2025-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12053935/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143735546","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jun Wang, Yang Li, Yisheng Wang, Guoli Wang, Chenyang Zhao, Ying Zhang, Haojie Lu
{"title":"Comparison of Protein Solubilization and Normalization Methods for Proteomics Analysis of Extracellular Vesicles from Urine.","authors":"Jun Wang, Yang Li, Yisheng Wang, Guoli Wang, Chenyang Zhao, Ying Zhang, Haojie Lu","doi":"10.1021/acs.jproteome.4c01085","DOIUrl":"10.1021/acs.jproteome.4c01085","url":null,"abstract":"<p><p>Extracellular vesicles (EVs) play a vital role in numerous biological processes. Proteomic research of EVs is crucial for understanding their functions and potential therapeutic implications. Despite many sample preparation protocols for mass spectrometry-based proteomics of EVs being described, the variability in protein extraction across different protocols has not been extensively investigated. Moreover, given the inherent heterogeneity of EVs, it is vital to conduct a thorough evaluation of normalization methods. Here, we present a comprehensive comparison of three widely used lysis agents─sodium dodecyl sulfate (SDS), urea, and sodium deoxycholate (SDC)─for protein extraction from EVs. We also assess the impact of different normalization strategies on protein quantification, which is crucial for ensuring reliable results. Our results show that method-dependent differences in protein recovery were observed, particularly for membrane-associated proteins. We also find that common normalization strategies, such as urine creatinine and EV markers, did not significantly stabilize protein quantification, indicating that these methods are not universally applicable as normalization standards. Our work thereby provides a reference for the selection of MS sample preparation and normalization strategies for a given EV proteomics project.</p>","PeriodicalId":48,"journal":{"name":"Journal of Proteome Research","volume":" ","pages":"2430-2442"},"PeriodicalIF":3.8,"publicationDate":"2025-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143784369","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Asia Botto, Chiara De Cesari, Noa Ndimurwanko, Francesco Finamore, Francesco Greco, Valentina Cappello, Valentina Casieri, Benoit Immordino, Vincenzo Lionetti, Mauro Gemmi, Ilaria Tonazzini, Elisa Giovannetti, Liam A McDonnell
{"title":"Novel PPT+SEC Workflow for High-Sensitivity Extracellular Vesicle Proteomics from Cell Media.","authors":"Asia Botto, Chiara De Cesari, Noa Ndimurwanko, Francesco Finamore, Francesco Greco, Valentina Cappello, Valentina Casieri, Benoit Immordino, Vincenzo Lionetti, Mauro Gemmi, Ilaria Tonazzini, Elisa Giovannetti, Liam A McDonnell","doi":"10.1021/acs.jproteome.5c00082","DOIUrl":"https://doi.org/10.1021/acs.jproteome.5c00082","url":null,"abstract":"<p><p>Size exclusion chromatography (SEC) is a well-established method for the isolation of extracellular vesicles (EVs), but the large elution volumes necessitate a concentration step prior to proteomics analysis. This concentration step can lead to a significant EV loss. Here we report an EV proteomics approach that enables the isolation of EVs into just 80 μL, which is directly compatible with proteomics analysis without the need for a prior concentration. EVs were characterized by transmission electron microscopy, Western blot, and nanoparticle tracking analysis, all of which confirmed the presence of small EVs. Proteomics analysis of the EVs was performed and benchmarked against those isolated by using an automated UHPLC-SEC platform. The novel workflow identified more proteins and more EV markers, including 96 of the 100 top exosomal proteins from the ExoCarta database, compared to 91 identified using EV samples isolated by UHPLC-SEC. When applied to EVs isolated from pancreatic cancer cell lines, the workflow demonstrated higher sensitivity for previously reported EV markers of pancreatic cancer.</p>","PeriodicalId":48,"journal":{"name":"Journal of Proteome Research","volume":" ","pages":""},"PeriodicalIF":3.8,"publicationDate":"2025-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143954720","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
David Teschner, David Gomez-Zepeda, Mateusz K Łącki, Thomas Kemmer, Anne Busch, Stefan Tenzer, Andreas Hildebrandt
{"title":"Rustims: An Open-Source Framework for Rapid Development and Processing of timsTOF Data-Dependent Acquisition Data.","authors":"David Teschner, David Gomez-Zepeda, Mateusz K Łącki, Thomas Kemmer, Anne Busch, Stefan Tenzer, Andreas Hildebrandt","doi":"10.1021/acs.jproteome.4c00966","DOIUrl":"https://doi.org/10.1021/acs.jproteome.4c00966","url":null,"abstract":"<p><p>Mass spectrometry is essential for analyzing and quantifying biological samples. The timsTOF platform is a prominent commercial tool for this purpose, particularly in bottom-up acquisition scenarios. The additional ion mobility dimension requires more complex data processing, yet most current software solutions for timsTOF raw data are proprietary or closed-source, limiting integration into custom workflows. We introduce rustims, a framework implementing a flexible toolbox designed for processing timsTOF raw data, currently focusing on data-dependent acquisition (DDA-PASEF). The framework employs a dual-language approach, combining efficient, multithreaded Rust code with an easy-to-use Python interface. This allows for implementations that are fast, intuitive, and easy to integrate. With imspy as its main Python scripting interface and sagepy for Sage search engine bindings, rustims enables fast, integrable, and intuitive processing. We demonstrate its capabilities with a pipeline for DDA-PASEF data including rescoring and integration of third-party tools like the Prosit intensity predictor and an extended ion mobility model. This pipeline supports tryptic proteomics and nontryptic immunopeptidomics data, with benchmark comparisons to FragPipe and PEAKS. Rustims is available on GitHub under the MIT license, with installation packages for multiple platforms on PyPi and all analysis scripts accessible via Zenodo.</p>","PeriodicalId":48,"journal":{"name":"Journal of Proteome Research","volume":"24 5","pages":"2358-2368"},"PeriodicalIF":3.8,"publicationDate":"2025-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12053931/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143955026","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Lauren Fields, Hannah N Miles, Alexis E Adrian, Elliot Patrenets, William A Ricke, Lingjun Li
{"title":"MSIght: A Modular Platform for Improved Confidence in Global, Untargeted Mass Spectrometry Imaging Annotation.","authors":"Lauren Fields, Hannah N Miles, Alexis E Adrian, Elliot Patrenets, William A Ricke, Lingjun Li","doi":"10.1021/acs.jproteome.4c01140","DOIUrl":"10.1021/acs.jproteome.4c01140","url":null,"abstract":"<p><p>Mass spectrometry imaging (MSI) has gained popularity in clinical analyses due to its high sensitivity, specificity, and throughput. However, global profiling experiments are often still restricted to LC-MS/MS analyses that lack spatial localization due to low-throughput methods for on-tissue peptide identification and confirmation. Additionally, the integration of parallel LC-MS/MS peptide confirmation, as well as histological stains for accurate mapping of identifications, presents a large bottleneck for data analysis, limiting throughput for untargeted profiling experiments. Here, we present a novel platform, termed MSIght, which automates the integration of these multiple modalities into an accessible and modular platform. Histological stains of tissue sections are coregistered to their respective MSI data sets to improve spatial localization and resolution of identified peptides. MS/MS peptide identifications via untargeted LC-MS/MS are used to confirm putative MSI identifications, thus generating MS images with greater confidence in a high-throughput, global manner. This platform has the potential to enable large-scale clinical cohorts to utilize MSI in the future for global proteomic profiling that uncovers novel biomarkers in a spatially resolved manner, thus widely expanding the utility of MSI in clinical discovery.</p>","PeriodicalId":48,"journal":{"name":"Journal of Proteome Research","volume":" ","pages":"2478-2490"},"PeriodicalIF":3.8,"publicationDate":"2025-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12097482/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143802040","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}