Molecular & Cellular Proteomics最新文献

{"title":"Immunopeptidomics Mapping of Listeria monocytogenes T Cell Epitopes in Mice.","authors":"Adillah Gul, Lecia L Pewe, Patrick Willems, Rupert Mayer, Fabien Thery, Caroline Asselman, Ilke Aernout, Rein Verbeke, Denzel Eggermont, Laura Van Moortel, Ellen Upton, Yifeng Zhang, Katie Boucher, Laia Miret-Casals, Hans Demol, Stefaan C De Smedt, Ine Lentacker, Lilliana Radoshevich, John T Harty, Francis Impens","doi":"10.1016/j.mcpro.2024.100829","DOIUrl":"10.1016/j.mcpro.2024.100829","url":null,"abstract":"<p><p>Listeria monocytogenes is a foodborne intracellular bacterial model pathogen. Protective immunity against Listeria depends on an effective CD8⁺ T cell response, but very few T cell epitopes are known in mice as a common animal infection model for listeriosis. To identify epitopes, we screened for Listeria immunopeptides presented in the spleen of infected mice by mass spectrometry-based immunopeptidomics. We mapped more than 6000 mouse self-peptides presented on MHC class I molecules, including 12 high confident Listeria peptides from 12 different bacterial proteins. Bacterial immunopeptides with confirmed fragmentation spectra were further tested for their potential to activate CD8⁺ T cells, revealing VTYNYINI from the putative cell wall surface anchor family protein LMON_0576 as a novel bona fide peptide epitope. The epitope showed high biological potency in a prime boost model and can be used as a research tool to probe CD8⁺ T cell responses in the mouse models of Listeria infection. Together, our results demonstrate the power of immunopeptidomics for bacterial antigen identification.</p>","PeriodicalId":18712,"journal":{"name":"Molecular & Cellular Proteomics","volume":" ","pages":"100829"},"PeriodicalIF":6.1,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11414675/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141988343","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}

{"title":"Secretome Analysis Using Affinity Proteomics and Immunoassays: A Focus on Tumor Biology.","authors":"Vanessa M Beutgen, Veronika Shinkevich, Johanna Pörschke, Celina Meena, Anna M Steitz, Elke Pogge von Strandmann, Johannes Graumann, María Gómez-Serrano","doi":"10.1016/j.mcpro.2024.100830","DOIUrl":"10.1016/j.mcpro.2024.100830","url":null,"abstract":"<p><p>The study of the cellular secretome using proteomic techniques continues to capture the attention of the research community across a broad range of topics in biomedical research. Due to their untargeted nature, independence from the model system used, historically superior depth of analysis, as well as comparative affordability, mass spectrometry-based approaches traditionally dominate such analyses. More recently, however, affinity-based proteomic assays have massively gained in analytical depth, which together with their high sensitivity, dynamic range coverage as well as high throughput capabilities render them exquisitely suited to secretome analysis. In this review, we revisit the analytical challenges implied by secretomics and provide an overview of affinity-based proteomic platforms currently available for such analyses, using the study of the tumor secretome as an example for basic and translational research.</p>","PeriodicalId":18712,"journal":{"name":"Molecular & Cellular Proteomics","volume":" ","pages":"100830"},"PeriodicalIF":6.1,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11417252/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141988345","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}

{"title":"Variation of Site-Specific Glycosylation Profiles of Recombinant Influenza Glycoproteins.","authors":"Zachary C Goecker, Meghan C Burke, Concepcion A Remoroza, Yi Liu, Yuri A Mirokhin, Sergey L Sheetlin, Dmitrii V Tchekhovskoi, Xiaoyu Yang, Stephen E Stein","doi":"10.1016/j.mcpro.2024.100827","DOIUrl":"10.1016/j.mcpro.2024.100827","url":null,"abstract":"<p><p>This work presents a detailed determination of site-specific N-glycan distributions of the recombinant influenza glycoproteins hemagglutinin (HA) and neuraminidase. Variation in glycosylation among recombinant glycoproteins is not predictable and can depend on details of the biomanufacturing process as well as details of protein structure. In this study, recombinant influenza proteins were analyzed from eight strains of four different suppliers. These include five HA and three neuraminidase proteins, each produced from a HEK293 cell line. Digestion was conducted using a series of complex multienzymatic methods designed to isolate glycopeptides containing single N-glycosylated sites. Site-specific glycosylation profiles of intact glycopeptides were produced using a recently developed method and comparisons were made using spectral similarity scores. Variation in glycan abundances and distribution was most pronounced between different strains of virus (similarity score = 383 out of 999), whereas digestion replicates and injection replicates showed relatively little variation (similarity score = 957). Notably, glycan distributions for homologous regions of influenza glycoprotein variants showed low variability. Due to the multiple possible sources of variation and inherent analytical difficulties in site-specific glycan determinations, variations were individually examined for multiple factors, including differences in supplier, production batch, protease digestion, and replicate measurement. After comparing all glycosylation distributions, four distinguishable classes could be identified for the majority of sites. Finally, attempts to identify glycosylation distributions on adjacent potential N-glycosylated sites of one HA variant were made. Only the second site (NnST) was found to be occupied using two rarely used proteases in proteomics, subtilisin and esperase, both of which did selectively cleave these adjacent sites.</p>","PeriodicalId":18712,"journal":{"name":"Molecular & Cellular Proteomics","volume":" ","pages":"100827"},"PeriodicalIF":6.1,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11417209/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141917120","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}

{"title":"One-step N-Terminomics Based on Isolation of Protein N-Terminal Peptides From LysargiNase Digests by Tip-Based Strong Cation Exchange Chromatography.","authors":"Kazuya Morikawa, Hiroshi Nishida, Koshi Imami, Yasushi Ishihama","doi":"10.1016/j.mcpro.2024.100820","DOIUrl":"10.1016/j.mcpro.2024.100820","url":null,"abstract":"<p><p>We have developed a one-step isolation method for protein N-terminal peptides from LysargiNase digests by pipette tip-based strong cation exchange (SCX) chromatography. This CHAMP-N (CHromatographic AMplification of Protein N-terminal peptides) method using disposable and parallel-processable SCX tips instead of conventional HPLC SCX columns facilitates simple, sensitive, reproducible, and high-throughput N-terminomic profiling without sacrificing the high identification numbers and selectivity achieved by the HPLC-based method. By applying the CHAMP-N method to HEK293T cells, we identified novel cleavage sites for signal and transit peptides and non-canonical translation initiation sites. Finally, for proteome-wide terminomics, we present a simple and comprehensive N- and C-terminomics platform employing three different tip-based approaches, including CHAMP-N, in which protease digestion and one-step isolation by tip LC are commonly used to achieve complementary terminome coverages.</p>","PeriodicalId":18712,"journal":{"name":"Molecular & Cellular Proteomics","volume":" ","pages":"100820"},"PeriodicalIF":6.1,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11382313/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141788629","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}

{"title":"GRable Version 1.0: A Software Tool for Site-Specific Glycoform Analysis With Improved MS1-Based Glycopeptide Detection With Parallel Clustering and Confidence Evaluation With MS2 Information.","authors":"Chiaki Nagai-Okatani, Daisuke Tominaga, Azusa Tomioka, Hiroaki Sakaue, Norio Goda, Shigeru Ko, Atsushi Kuno, Hiroyuki Kaji","doi":"10.1016/j.mcpro.2024.100833","DOIUrl":"10.1016/j.mcpro.2024.100833","url":null,"abstract":"<p><p>High-throughput intact glycopeptide analysis is crucial for elucidating the physiological and pathological status of the glycans attached to each glycoprotein. Mass spectrometry-based glycoproteomic methods are challenging because of the diversity and heterogeneity of glycan structures. Therefore, we developed an MS1-based site-specific glycoform analysis method named \"Glycan heterogeneity-based Relational IDentification of Glycopeptide signals on Elution profile (Glyco-RIDGE)\" for a more comprehensive analysis. This method detects glycopeptide signals as a cluster based on the mass and chromatographic properties of glycopeptides and then searches for each combination of core peptides and glycan compositions by matching their mass and retention time differences. Here, we developed a novel browser-based software named GRable for semi-automated Glyco-RIDGE analysis with significant improvements in glycopeptide detection algorithms, including \"parallel clustering.\" This unique function improved the comprehensiveness of glycopeptide detection and allowed the analysis to focus on specific glycan structures, such as pauci-mannose. The other notable improvement is evaluating the \"confidence level\" of the GRable results, especially using MS2 information. This function facilitated reduced misassignment of the core peptide and glycan composition and improved the interpretation of the results. Additional improved points of the algorithms are \"correction function\" for accurate monoisotopic peak picking; one-to-one correspondence of clusters and core peptides even for multiply sialylated glycopeptides; and \"inter-cluster analysis\" function for understanding the reason for detected but unmatched clusters. The significance of these improvements was demonstrated using purified and crude glycoprotein samples, showing that GRable allowed site-specific glycoform analysis of intact sialylated glycoproteins on a large-scale and in-depth. Therefore, this software will help us analyze the status and changes in glycans to obtain biological and clinical insights into protein glycosylation by complementing the comprehensiveness of MS2-based glycoproteomics. GRable can be freely run online using a web browser via the GlyCosmos Portal (https://glycosmos.org/grable).</p>","PeriodicalId":18712,"journal":{"name":"Molecular & Cellular Proteomics","volume":" ","pages":"100833"},"PeriodicalIF":6.1,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11421343/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142056092","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}

{"title":"MIB2 Functions in Oocyte Meiosis by Modulating Chromatin Configuration.","authors":"Yifei Jin, Guangyi Sun, Jiashuo Li, Qing Cheng, Hongzheng Sun, Longsen Han, Xuejiang Guo, Shuai Zhu, Qiang Wang","doi":"10.1016/j.mcpro.2024.100813","DOIUrl":"10.1016/j.mcpro.2024.100813","url":null,"abstract":"<p><p>Chromatin configuration serves as a principal indicator of GV (germinal vesicle)-stage oocyte quality. However, the underlying mechanisms governing the chromatin configuration transition from NSN (non-surrounded nucleolus) to SN (surrounded nucleolus) remain unclear. In this study, by conducting a quantitative proteomic analysis, we identified an increased expression of the MIB2 (MIB E3 ubiquitin protein ligase 2) protein in SN oocytes. Specific depletion of MIB2 in SN oocytes not only leads to severe disruption of the meiotic apparatus and a higher incidence of aneuploidy but also adversely affects meiotic maturation and early embryo development. Notably, overexpression of MIB2 in NSN oocytes facilitates the chromatin configuration transition. Meantime, we observed that forced expression of MIB2 in NSN oocytes significantly mitigates spindle/chromosome disorganization and aneuploidy. In summary, our results suggest that chromatin configuration transition regulated by MIB2 is crucial for oocytes to acquire developmental competence.</p>","PeriodicalId":18712,"journal":{"name":"Molecular & Cellular Proteomics","volume":" ","pages":"100813"},"PeriodicalIF":6.1,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11364126/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141633940","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}

{"title":"Data-Independent Acquisition: A Milestone and Prospect in Clinical Mass Spectrometry-Based Proteomics.","authors":"Klemens Fröhlich, Matthias Fahrner, Eva Brombacher, Adrianna Seredynska, Maximilian Maldacker, Clemens Kreutz, Alexander Schmidt, Oliver Schilling","doi":"10.1016/j.mcpro.2024.100800","DOIUrl":"10.1016/j.mcpro.2024.100800","url":null,"abstract":"<p><p>Data-independent acquisition (DIA) has revolutionized the field of mass spectrometry (MS)-based proteomics over the past few years. DIA stands out for its ability to systematically sample all peptides in a given m/z range, allowing an unbiased acquisition of proteomics data. This greatly mitigates the issue of missing values and significantly enhances quantitative accuracy, precision, and reproducibility compared to many traditional methods. This review focuses on the critical role of DIA analysis software tools, primarily focusing on their capabilities and the challenges they address in proteomic research. Advances in MS technology, such as trapped ion mobility spectrometry, or high field asymmetric waveform ion mobility spectrometry require sophisticated analysis software capable of handling the increased data complexity and exploiting the full potential of DIA. We identify and critically evaluate leading software tools in the DIA landscape, discussing their unique features, and the reliability of their quantitative and qualitative outputs. We present the biological and clinical relevance of DIA-MS and discuss crucial publications that paved the way for in-depth proteomic characterization in patient-derived specimens. Furthermore, we provide a perspective on emerging trends in clinical applications and present upcoming challenges including standardization and certification of MS-based acquisition strategies in molecular diagnostics. While we emphasize the need for continuous development of software tools to keep pace with evolving technologies, we advise researchers against uncritically accepting the results from DIA software tools. Each tool may have its own biases, and some may not be as sensitive or reliable as others. Our overarching recommendation for both researchers and clinicians is to employ multiple DIA analysis tools, utilizing orthogonal analysis approaches to enhance the robustness and reliability of their findings.</p>","PeriodicalId":18712,"journal":{"name":"Molecular & Cellular Proteomics","volume":" ","pages":"100800"},"PeriodicalIF":6.1,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11380018/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141331433","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}

{"title":"Chemo-Phosphoproteomic Profiling with ATR Inhibitors Berzosertib and Gartisertib Uncovers New Biomarkers and DNA Damage Response Regulators.","authors":"Rathan Jadav, Florian Weiland, Sylvie M Noordermeer, Thomas Carroll, Yuandi Gao, Jianming Wang, Houjiang Zhou, Frederic Lamoliatte, Rachel Toth, Thomas Macartney, Fiona Brown, C James Hastie, Constance Alabert, Haico van Attikum, Frank Zenke, Jean-Yves Masson, John Rouse","doi":"10.1016/j.mcpro.2024.100802","DOIUrl":"10.1016/j.mcpro.2024.100802","url":null,"abstract":"<p><p>The ATR kinase protects cells against DNA damage and replication stress and represents a promising anti-cancer drug target. The ATR inhibitors (ATRi) berzosertib and gartisertib are both in clinical trials for the treatment of advanced solid tumors as monotherapy or in combination with genotoxic agents. We carried out quantitative phospho-proteomic screening for ATR biomarkers that are highly sensitive to berzosertib and gartisertib, using an optimized mass spectrometry pipeline. Screening identified a range of novel ATR-dependent phosphorylation events, which were grouped into three broad classes: (i) targets whose phosphorylation is highly sensitive to ATRi and which could be the next generation of ATR biomarkers; (ii) proteins with known genome maintenance roles not previously known to be regulated by ATR; (iii) novel targets whose cellular roles are unclear. Class iii targets represent candidate DNA damage response proteins and, with this in mind, proteins in this class were subjected to secondary screening for recruitment to DNA damage sites. We show that one of the proteins recruited, SCAF1, interacts with RNAPII in a phospho-dependent manner and recruitment requires PARP activity and interaction with RNAPII. We also show that SCAF1 deficiency partly rescues RAD51 loading in cells lacking the BRCA1 tumor suppressor. Taken together these data reveal potential new ATR biomarkers and new genome maintenance factors.</p>","PeriodicalId":18712,"journal":{"name":"Molecular & Cellular Proteomics","volume":" ","pages":"100802"},"PeriodicalIF":6.1,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11338954/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141331431","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}

{"title":"Quantitative Phosphoproteomic Profiling of Mouse Sperm Maturation in Epididymis Revealed Kinases Important for Sperm Motility.","authors":"Xiangzheng Zhang, Haixia Tu, Xin Zhou, Bing Wang, Yueshuai Guo, Chenghao Situ, Yaling Qi, Yan Li, Xuejiang Guo","doi":"10.1016/j.mcpro.2024.100810","DOIUrl":"10.1016/j.mcpro.2024.100810","url":null,"abstract":"<p><p>Transcriptionally and translationally silent sperm undergo functional maturation during epididymis traverse, which provides sperm ability to move and is crucial for successful fertilization. However, the molecular mechanisms governing sperm maturation remain poorly understood, especially at the protein post-translational modification level. In this study, we conducted a comprehensive quantitative phosphoproteomic analysis of mouse epididymal sperm from different regions (caput, corpus, and cauda) to unveil the dynamics of protein phosphorylation during sperm maturation. We identified 6447 phosphorylation sites in 1407 phosphoproteins, and 345 phosphoproteins were differentially phosphorylated between caput and cauda sperm. Gene ontology and KEGG pathway analyses showed enrichment of differentially phosphorylated proteins in energy metabolism, sperm motility, and fertilization. Kinase substrate network analysis followed by inhibition assay and quantitative phosphoproteomics analysis showed that TSSK2 kinase is important for sperm motility and progressive motility. This study systemically characterized the intricate phosphorylation regulation during sperm maturation in the mouse epididymis, which can be a basis to elucidate sperm motility acquisition, and to offer potential targets for male contraception and the treatment of male infertility.</p>","PeriodicalId":18712,"journal":{"name":"Molecular & Cellular Proteomics","volume":" ","pages":"100810"},"PeriodicalIF":6.1,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11338950/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141559242","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}

{"title":"DIA-Based Phosphoproteomics Identifies Early Phosphorylation Events in Response to EGTA and Mannitol in Arabidopsis.","authors":"Tian Sang, Chin-Wen Chen, Zhen Lin, Yu Ma, Yanyan Du, Pei-Yi Lin, Marco Hadisurya, Jian-Kang Zhu, Zhaobo Lang, W Andy Tao, Chuan-Chih Hsu, Pengcheng Wang","doi":"10.1016/j.mcpro.2024.100804","DOIUrl":"10.1016/j.mcpro.2024.100804","url":null,"abstract":"<p><p>Osmotic stress significantly hampers plant growth and crop yields, emphasizing the need for a thorough comprehension of the underlying molecular responses. Previous research has demonstrated that osmotic stress rapidly induces calcium influx and signaling, along with the activation of a specific subset of protein kinases, notably the Raf-like protein (RAF)-sucrose nonfermenting-1-related protein kinase 2 (SnRK2) kinase cascades within minutes. However, the intricate interplay between calcium signaling and the activation of RAF-SnRK2 kinase cascades remains elusive. Here, in this study, we discovered that Raf-like protein (RAF) kinases undergo hyperphosphorylation in response to osmotic shocks. Intriguingly, treatment with the calcium chelator EGTA robustly activates RAF-SnRK2 cascades, mirroring the effects of osmotic treatment. Utilizing high-throughput data-independent acquisition-based phosphoproteomics, we unveiled the global impact of EGTA on protein phosphorylation. Beyond the activation of RAFs and SnRK2s, EGTA treatment also activates mitogen-activated protein kinase cascades, Calcium-dependent protein kinases, and receptor-like protein kinases, etc. Through overlapping assays, we identified potential roles of mitogen-activated protein kinase kinase kinase kinases and receptor-like protein kinases in the osmotic stress-induced activation of RAF-SnRK2 cascades. Our findings illuminate the regulation of phosphorylation and cellular events by Ca²⁺ signaling, offering insights into the (exocellular) Ca²⁺ deprivation during early hyperosmolality sensing and signaling.</p>","PeriodicalId":18712,"journal":{"name":"Molecular & Cellular Proteomics","volume":" ","pages":"100804"},"PeriodicalIF":6.1,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11325057/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141432316","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}