Matthieu Sanial, Ryan Miled, Marine Alves, Sandra Claret, Nicolas Joly, Véronique Proux-Gillardeaux, Anne Plessis, Sébastien Léon
{"title":"Direct observation of fluorescent proteins in gels: A rapid, cost-efficient, and quantitative alternative to immunoblotting","authors":"Matthieu Sanial, Ryan Miled, Marine Alves, Sandra Claret, Nicolas Joly, Véronique Proux-Gillardeaux, Anne Plessis, Sébastien Léon","doi":"10.1111/boc.202400161","DOIUrl":"https://doi.org/10.1111/boc.202400161","url":null,"abstract":"<div>\u0000 \u0000 \u0000 <section>\u0000 \u0000 <h3> Background Information</h3>\u0000 \u0000 <p>The discovery of green fluorescent protein (GFP) and its derivatives has revolutionized cell biology. These fluorescent proteins (FPs) have enabled the real-time observation of protein localization and dynamics within live cells. Applications of FP vary from monitoring gene/protein expression patterns, visualizing protein-protein interactions, measuring protein stability, assessing protein mobility, and creating biosensors. The utility of FPs also extends to biochemical approaches through immunoblotting and proteomic analyses, aided by anti-FP antibodies and nanobodies. FPs are notoriously robust proteins with a tightly folded domain that confers a strong stability and a relative resistance to degradation and denaturation.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Methods and Results</h3>\u0000 \u0000 <p>In this study, we report that various green, orange, and red FPs can be maintained in a native, fluorescent state during the entire process of protein sample extraction, incubation with sample buffer, loading, and migration on SDS-PAGE (sodium dodecyl sulfate-polyacrylamide gel electrophoresis) with only minor adaptations of traditional protocols. This protocol results in the ability to detect and quantify in-gel fluorescence (IGF) of endogenously-expressed proteins tagged with FPs directly after migration, using standard fluorescence-imaging devices. This approach eliminates the need for antibodies and chemiluminescent reagents, as well as the time-consuming steps inherent in immunoblotting such as transfer onto a membrane and antibody incubations.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Conclusions and Significance</h3>\u0000 \u0000 <p>Overall, IGF detection provides clearer data with less background interference, a sensitivity comparable to or better than antibody-based detection, a better quantification, and a broader dynamic range. After fluorescence imaging, gels can still be used for other applications such as total protein staining or immunoblotting if needed. It also expands possibilities by allowing the detection of FPs for which antibodies are not available. Our study explores the feasibility, limitations, and applications of IGF for detecting endogenously expressed proteins in cell extracts, providing insights into sample preparation, imaging conditions, and sensitivity optimizations, and potential applications such as co-immunoprecipitation experiments.</p>\u0000 </section>\u0000 </div>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":"117 2","pages":""},"PeriodicalIF":2.4,"publicationDate":"2025-02-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/boc.202400161","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143379976","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Lung tumor organoids migrate as cell clusters containing cancer stem cells under hypoxic condition","authors":"Yanjiao Li, Jiarong Zou, Yanhua Fang, Jianing Zuo, Ruoyu Wang, Shanshan Liang","doi":"10.1111/boc.202400081","DOIUrl":"https://doi.org/10.1111/boc.202400081","url":null,"abstract":"<div>\u0000 \u0000 \u0000 <section>\u0000 \u0000 <h3> Background</h3>\u0000 \u0000 <p>Tumor hypoxia reshapes the microenvironment, driving progression, invasion, metastasis, and therapy resistance. Patient-derived tumor organoids, formed under three-dimensional conditions, preserve cellular heterogeneity and nutrient gradients, making them ideal for studying hypoxia-induced tumor responses. This study examines hypoxia-induced changes in lung tumor organoids from two patients, focusing on tumor-associated markers, stem cell markers, and migration capabilities.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Results</h3>\u0000 \u0000 <p>Our findings demonstrate that hypoxia distinctively modulates the expression of lung cancer markers thyroid transcription factor-1, cytokeratin 7, and ΔNP63 variant. Hypoxia also induces the upregulation of stem cell-associated markers, resulting in an increased proportion of cancer stem cells. Furthermore, hypoxic lung tumor organoids exhibit unique migratory behavior upon reoxygenation, driven by epithelial-mesenchymal transition and the elevated expression of matrix metalloproteinases 7 and matrix metalloproteinases 9, indicating their enhanced invasive potential.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Conclusions</h3>\u0000 \u0000 <p>These findings highlight the value of lung tumor organoids as models for studying hypoxia's complex role in lung cancer. Hypoxia significantly modulates lung tumor organoids growth, stemness, and migratory behavior, providing critical insights into tumor progression and therapy resistance.</p>\u0000 </section>\u0000 </div>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":"117 2","pages":""},"PeriodicalIF":2.4,"publicationDate":"2025-02-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143379978","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ebru Karakaş Sarıkaya, Suray Pehlivanoğlu, Merve Özcan Türkmen, Yavuz Ekincioğlu, Feyza Kostak, Sultan Çelik, Ömer Dereli
{"title":"Anticancer (cytotoxic, anticlonogenic, antimetastatic, immunomodulatory actions) properties of 3,5-dibromosalicylaldehyde against glioblastoma cells and DFT analyses (FT-IR, Raman, NMR, UV) as well as a molecular docking study","authors":"Ebru Karakaş Sarıkaya, Suray Pehlivanoğlu, Merve Özcan Türkmen, Yavuz Ekincioğlu, Feyza Kostak, Sultan Çelik, Ömer Dereli","doi":"10.1111/boc.202400138","DOIUrl":"https://doi.org/10.1111/boc.202400138","url":null,"abstract":"<div>\u0000 \u0000 \u0000 <section>\u0000 \u0000 <h3> Background Information</h3>\u0000 \u0000 <p>The primary objectives of this study were to characterize 3,5-dibromosalicylaldehyde (3,5-DBSA) and, investigate its antiproliferative, antimetastatic, cytotoxic, and immunoregulatory properties. NMR, Raman, UV, and FT-IR spectroscopies were used to characterize 3,5-DBSA. Potential conformations of 3,5-DBSA were evaluated using Spartan's MMFF method. Geometry optimization calculations using Gaussian software calculated conformation energy values.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Results</h3>\u0000 \u0000 <p>Subsequently, Raman, FT-IR, UV (ethanol) and NMR (DMSO) parameters were calculated. The experimental spectrum was compared to theoretical spectroscopic data. The present investigation investigated 3,5-DBSA's anticancer properties; therefore, docking was done once the stable structure had been identified.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Conclusion</h3>\u0000 \u0000 <p>Identifying stable structure is crucial to molecular docking studies. In order to identify the mechanism by which 3,5-DBSA binds to PI3K as a therapeutic target, molecular docking was utilized. This work is the first to show that 3,5-DBSA is cytotoxic, anticlonogenic, antimetastatic, and immunomodulatory in glioblastoma cell line U87MG compared to healthy fibroblast L929 cells. Cytotoxicity and anti-clonogenicity studies investigated 3,5-DBSA's antiproliferative activities, whereas wound healing assays assessed cell migration. The immunomodulatory effects of 3,5-DBSA in glioblastoma were assessed by measuring Netrin-1 and IL-6 protein levels. According to our findings, 3,5-DBSA may treat glioblastoma.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Significance</h3>\u0000 \u0000 <p>This work analyzes 3,5-DBSA's conformational search, characterization, molecular docking, and structural and anticancer properties.</p>\u0000 </section>\u0000 </div>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":"117 2","pages":""},"PeriodicalIF":2.4,"publicationDate":"2025-02-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143379977","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"An interview with Alexis Lebecq. Winner of the French Society for Cell Biology (SBCF) thesis award 2023","authors":"Alexis Lebecq, Paul Trevorrow","doi":"10.1111/boc.202400162","DOIUrl":"10.1111/boc.202400162","url":null,"abstract":"","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":"117 1","pages":""},"PeriodicalIF":2.4,"publicationDate":"2025-02-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143078551","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Flotillins in membrane trafficking and physiopathology","authors":"Stéphane Bodin, Hadeer Elhabashy, Ewan Macdonald, Dominic Winter, Cécile Gauthier-Rouvière","doi":"10.1111/boc.202400134","DOIUrl":"10.1111/boc.202400134","url":null,"abstract":"<div>\u0000 \u0000 \u0000 <section>\u0000 \u0000 <p>Flotillin 1 and 2 are highly conserved and homologous members of the stomatin, prohibitin, flotillin, HflK/C (SPFH) family. These ubiquitous proteins assemble into hetero-oligomers at the cytoplasmic membrane in sphingolipid-enriched domains. Flotillins play crucial roles in various cellular processes, likely by concentrating sphingosine. They primarily act as scaffolding protein complexes within membrane microdomains (also called lipid rafts) and induce endocytosis and trafficking. Their diverse cargos in the upregulated flotillin–induced trafficking (UFIT) pathway, including tyrosine kinase receptors, adhesion molecules, and neurotransmitter receptors, link them to a wide range of cellular processes and diseases. Consequently, flotillin upregulation has been associated with various pathological conditions such as cancer, metabolic disorders, and neurodegenerative diseases. Flotillins may also be co-opted by pathogens to facilitate their entry and growth within host cells.</p>\u0000 \u0000 <p>In this review, we examined recent advancements in elucidating the structure and functions of the flotillin protein complex, including its implications in favoring the generation of sphingosine 1-phosphate, an essential bioactive lipid. We emphasized how the recent cryo-electron microscopy (cryo-EM) structure of a truncated cone-shaped cage composed of 22 copies of flotillin 1 and 2 subunits has enhanced our understanding of the flotillin complex organization within membrane microdomains and its role in membrane remodeling. We also explored how flotillin upregulation can perturb endosomal trafficking and contribute to various pathologies.</p>\u0000 \u0000 <p>A comprehensive understanding of flotillin oligomer organization and function is crucial to developing targeted therapies for diseases associated with flotillin overexpression.</p>\u0000 </section>\u0000 </div>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":"117 1","pages":""},"PeriodicalIF":2.4,"publicationDate":"2025-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11775717/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143057866","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Revealing mitochondrial architecture and functions with single molecule localization microscopy","authors":"Nicolas Jolivet, Giulia Bertolin","doi":"10.1111/boc.202400082","DOIUrl":"10.1111/boc.202400082","url":null,"abstract":"<p>Understanding the spatiotemporal organization of components within living systems requires the highest resolution possible. Microscopy approaches that allow for a resolution below 250 nm include electron and super-resolution microscopy (SRM). The latter combines advanced imaging techniques and the optimization of image processing methods. Over the last two decades, various SRM-related approaches have been introduced, especially those relying on single molecule localization microscopy (SMLM). To develop and apply SMLM approaches, mitochondria are an ideal cellular compartment due to their size, which is below the standard diffraction limit. Furthermore, mitochondria are a dynamic yet narrow compartment, and a resolution below 250 nm is required to study their composition and multifaceted functions. To this end, several SMLM technologies have been used to reveal mitochondrial composition. However, there is still room for improvement in existing techniques to study protein–protein interactions and protein dynamics within this compartment. This review aims to offer an updated overview of the existing SMLM techniques and probes associated with mitochondria to enhance their resolution at the nanoscale. Last, it paves the way for future SMLM improvements to better resolve mitochondrial dynamics and functions.</p>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":"117 1","pages":""},"PeriodicalIF":2.4,"publicationDate":"2025-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11775716/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143057868","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Maxence Gaillard, Charles H. Pence, Mylène Botbol-Baum
{"title":"Organoid Ethical Typology: varieties of three-dimensional stem cell constructs and the many issues they raise in bioethics","authors":"Maxence Gaillard, Charles H. Pence, Mylène Botbol-Baum","doi":"10.1111/boc.202400093","DOIUrl":"10.1111/boc.202400093","url":null,"abstract":"<p>The advancement of and prospects for stem cell research raise a number of specific ethical issues. While navigating the ethical landscape of stem cell research is often challenging for biology researchers and biotechnology innovators, it is also difficult for the public and other persons of concern (from ethicists to policy-makers) to grasp the technicalities of a burgeoning field that develops in many directions. Organoids are one of these new biotechnological constructs that are currently eliciting a rich debate in bioethics. In this guide, we argue that different types of organoids have different emerging properties with different ethical implications. Going from general properties to particular ones, we propose a typology of organoid technology and other associated biotechnology from a philosophical and ethical perspective. We point to relevant ethical issues and try to convey the sense of uncertainty peculiar to ongoing research and emerging technological objects.</p>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":"117 1","pages":""},"PeriodicalIF":2.4,"publicationDate":"2025-01-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11758490/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143031967","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Caroline Soulet, Jordi Josa-Castro, María Moriel-Carretero
{"title":"Neutral lipids restrict the mobility of broken DNA molecules during comet assays","authors":"Caroline Soulet, Jordi Josa-Castro, María Moriel-Carretero","doi":"10.1111/boc.202400141","DOIUrl":"10.1111/boc.202400141","url":null,"abstract":"<p>One widespread technique to assess in relative terms the amount of broken DNA present in the genome of individual cells consists of immobilizing the cell's nucleus under an agarose pad (called the nucleoid) and subjecting the whole genome to electrophoresis to force broken DNA molecules out of it. Since the migrating broken DNA molecules create a tail behind the nucleoid, this technique is named the comet assay. While performing comet assays regularly, we systematically observed circular regions devoid of DNA within the nucleoid region. We characterize here that these correspond to clusters of neutral (apolar) lipids, since they could be labeled with neutral lipid-dying molecules, increased when cells were fed with oleic acid, and were irresponsive to the electrophoretic field. Of relevance, de-lipidation assays, either in vivo, or in vitro using acetone, show that these neutral lipids (NL) within the nucleoid limit the ability of broken DNA molecules to migrate into the comet tail. From a technical point of view, we show that de-lipidation permits a wider range for the detection of broken DNA molecules. Biologically, we put forward the notion that NL in contact with DNA may locally exert regulatory functions within the cell's nucleus.</p>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":"117 1","pages":""},"PeriodicalIF":2.4,"publicationDate":"2025-01-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11758471/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143031944","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Zahra Nashtahosseini, Masoumeh Nejatollahi, Ahmad Fazilat, Elahe Zarif Fakoor, Alireza Emamvirdizadeh, Kamran Bahadori, Niloofar Sadat Hadian, Mohammad Valilo
{"title":"The crosstalk between exosomal miRNA and ferroptosis: A narrative review","authors":"Zahra Nashtahosseini, Masoumeh Nejatollahi, Ahmad Fazilat, Elahe Zarif Fakoor, Alireza Emamvirdizadeh, Kamran Bahadori, Niloofar Sadat Hadian, Mohammad Valilo","doi":"10.1111/boc.202400077","DOIUrl":"10.1111/boc.202400077","url":null,"abstract":"<div>\u0000 \u0000 <section>\u0000 \u0000 \u0000 <p>Ferroptosis is a type of cell death that multiple mechanisms and pathways contribute to the positive and negative regulation of it. For example, increased levels of reactive oxygen species (ROS) induce ferroptosis. ferroptosis unlike apoptosis, it is not dependent on caspases, but is dependent on iron. Exosomes are membrane-bound vesicles with a size of about 30 to 150 nm, contain various cellular components, including DNA, RNA, microRNAs (miRNAs), lipids, and proteins, which are genetically similar to their cells of origin. Exosomes are found in all bodily fluids, including blood, saliva, and urine. Cells often release exosomes after their fusion with the cell membrane. They play an important role in immune regulation and cell-cell communication. miRNAs, which are noncoding RNAs with a length of about 18 to 24 nucleotides, are involved in regulating gene expression after transcription. Emerging data suggests that exosomal miRNAs are implicated in various pathophysiological mechanisms of cells, including metastasis, drug resistance, and cell death. In addition, functional studies have indicated that exosomal miRNAs can play a key role in the modulation of cell death by regulating ferroptosis. Therefore, in this review, given the importance of exosomal miRNAs in ferroptosis, we decided to elucidate the relationship between exosomal miRNAs and ferroptosis in various diseases.</p>\u0000 </section>\u0000 </div>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":"117 1","pages":""},"PeriodicalIF":2.4,"publicationDate":"2025-01-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143031972","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Héctor M. Alvarez, Mariana P. Lanfranconi, Martín A. Hernández
{"title":"Metabolism-lipid droplet-nucleic acid crosstalk to regulate lipid storage and other cellular processes in oleaginous Rhodococcus bacteria","authors":"Héctor M. Alvarez, Mariana P. Lanfranconi, Martín A. Hernández","doi":"10.1111/boc.202400094","DOIUrl":"10.1111/boc.202400094","url":null,"abstract":"<p>Actinobacteria belonging to <i>Mycobacterium</i> and <i>Rhodococcus</i> genera are able to synthesize and intracellularly accumulate variable amounts of triacylglycerols (TAG) in the form of lipid droplets (LDs). The lipid storage capacity of LDs in cells is controlled by the balance between lipogenesis and lipolysis. The growth of LDs in bacterial cells may be directly promoted by TAG biosynthesis, whereas TAG degradation might result in the reduction of LD sizes and lipid storage capacity. Therefore, LD formation and turnover have to be precisely regulated to maintain a balanced lipid distribution, coupling gene regulation with the metabolic state of the cell. In eukaryotic cells, LDs have emerged as critical mediators of diverse cellular responses, including fatty acid trafficking and modulation of transcriptional programs. Recent studies performed in mycobacteria and rhodococci suggested the existence of similar crosstalk mechanisms between lipid metabolism, LDs, and gene expression regulation in cells. This review connects and organizes results of different studies in a comprehensive framework for providing evidence of “lipid metabolism-LDs-genomic DNA” crosstalk occurring in TAG-accumulating actinobacteria. We provide examples indicating that bacterial cells evolved sensing mechanisms that detect lipid metabolites changes as indicators of metabolic states, and adapt their transcriptional profiles through epigenetic-like mechanisms mediated by LD-associated proteins. Here, we describe the molecular interconnections of this coupling system and the main role of each component that integrates the information about the cellular metabolic state into the regulation of lipogenesis, LD formation and transcription in oleaginous bacteria.</p>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":"117 1","pages":""},"PeriodicalIF":2.4,"publicationDate":"2025-01-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143031936","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}