Proteins-Structure Function and Bioinformatics最新文献

{"title":"Insight Into Factors Influencing the Aggregation Process in Wild-Type and P66R Mutant SOD1: Computational and Spectroscopic Approaches.","authors":"Roghayeh Farrokhzad, Bagher Seyedalipour, Payam Baziyar, Saman Hosseinkhani","doi":"10.1002/prot.26765","DOIUrl":"10.1002/prot.26765","url":null,"abstract":"<p><p>Disturbances in metal ion homeostasis associated with amyotrophic lateral sclerosis (ALS) have been described for several years, but the exact mechanism of involvement is not well understood. To elucidate the role of metalation in superoxide dismutase (SOD1) misfolding and aggregation, we comprehensively characterized the structural features (apo/holo forms) of WT-SOD1 and P66R mutant in loop IV. Using computational and experimental methodologies, we assessed the physicochemical properties of these variants and their correlation with protein aggregation at the molecular level. Modifications in apo-SOD1 compared to holo-SOD1 were more pronounced in flexibility, stability, hydrophobicity, and intramolecular interactions, as indicated by molecular dynamics simulations. The enzymatic activities of holo/apo-WT SOD1 were 1.30 and 1.88-fold of the holo/apo P66R mutant, respectively. Under amyloid-inducing conditions, decreased ANS fluorescence intensity in the apo-form relative to the holo-form suggested pre-fibrillar species and amyloid aggregate growth due to occluded hydrophobic pockets. FTIR spectroscopy revealed that apo-WT-SOD1 and apo-P66R exhibited a mixture of parallel and intermolecular β-sheet structures, indicative of aggregation propensity. Aggregate species were identified using TEM, Congo red staining, and ThT/ANS fluorescence spectroscopy. Thermodynamic analyses with GdnHCl demonstrated that metal deficit, mutation, and intramolecular disulfide bond reduction are essential for initiating SOD1 misfolding and aggregation. These disruptions destabilize the dimer-monomer equilibrium, promoting dimer dissociation into monomers and decreasing the thermodynamic stability of SOD1 variants, thus facilitating amyloid/amorphous aggregate formation. Our findings offer novel insights into protein aggregation mechanisms in disease pathology and highlight potential therapeutic strategies against toxic protein aggregation, including SOD1.</p>","PeriodicalId":56271,"journal":{"name":"Proteins-Structure Function and Bioinformatics","volume":" ","pages":"885-907"},"PeriodicalIF":3.2,"publicationDate":"2025-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142792732","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":"Unraveling GPCRs Allosteric Modulation. Cannabinoid 1 Receptor as a Case Study.","authors":"Alejandro Cruz, Arieh Warshel","doi":"10.1002/prot.26762","DOIUrl":"10.1002/prot.26762","url":null,"abstract":"<p><p>G-protein-coupled receptors (GPCRs) constitute one of the most prominent families of integral membrane receptor proteins that mediate most transmembrane signaling processes. Malfunction of these signal transduction processes is one of the underlying causes of many human pathologies (Parkinson's, Huntington's, heart diseases, etc), provoking that GPCRs are the largest family of druggable proteins. However, these receptors have been targeted traditionally by orthosteric ligands, which usually causes side effects due to the simultaneous targeting of homologous receptor subtypes. Allosteric modulation offers a promising alternative approach to circumvent this problematic and, thus, comprehending its details is a most important task. Here we use the Cannabinoid type-1 receptor (CB1R) in trying to shed light on this issue, focusing on positive allosteric modulation. This is done by using the protein-dipole Langevin-dipole (PDLD) within the linear response approximation (LRA) framework (PDLD/S-2000) along with our coarse-grained (CG) model of membrane proteins to evaluate the dissociation constants (K _Bs) and cooperativity factors (αs) for a diverse series of CB1R positive allosteric modulators belonging to the 2-phenylindole structural class, considering CP55940 as an agonist. The agreement with the experimental data evinces that significantly populated allosteric modulator:CB1R and allosteric modulator:CP55940:CB1R complexes have been identified and characterized successfully. Analyzing them, it has been determined that CB1R positive allosteric modulation lies in an outwards displacement of transmembrane α helix (TM) 4 extracellular end and in the regulation of the range of motion of a compound TM7 movement for binary and ternary complexes, respectively. In this respect, we achieved a better comprehension of the molecular architecture of CB1R positive allosteric site, identifying Lys192^3.28 and Gly194^3.30 as key residues regarding electrostatic interactions inside this cavity, and to rationalize (at both structural and molecular level) the exhibited stereoselectivity in relation to positive allosteric modulation activity by considered CB1R allosteric modulators. Additionally, putative/postulated allosteric binding sites have been screened successfully, identifying the real CB1R positive allosteric site, and most structure-activity relationship (SAR) studies of CB1R 2-phenylindole allosteric modulators have been rationalized. All these findings point out towards the predictive value of the methodology used in the current work, which can be applied to other biophysical systems of interest. The results presented in this study contribute significantly to understand GPCRs allosteric modulation and, hopefully, will encourage a more thorough exploration of the topic.</p>","PeriodicalId":56271,"journal":{"name":"Proteins-Structure Function and Bioinformatics","volume":" ","pages":"763-785"},"PeriodicalIF":3.2,"publicationDate":"2025-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11879764/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142711818","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":"The Crystal Structure of Human IgD-Fc Reveals Unexpected Differences With Other Antibody Isotypes.","authors":"Anna M Davies, Tam T T Bui, Raúl Pacheco-Gómez, Susan K Vester, Andrew J Beavil, Hannah J Gould, Brian J Sutton, James M McDonnell","doi":"10.1002/prot.26771","DOIUrl":"10.1002/prot.26771","url":null,"abstract":"<p><p>Of the five human antibody isotypes, the function of IgD is the least well-understood, although various studies point to a role for IgD in mucosal immunity. IgD is also the least well structurally characterized isotype. Until recently, when crystal structures were reported for the IgD Fab, the only structural information available was a model for intact IgD based on solution scattering data. We now report the crystal structure of human IgD-Fc solved at 3.0 Å resolution. Although similar in overall architecture to other human isotypes, IgD-Fc displays markedly different orientations of the Cδ3 domains in the Cδ3 domain dimer and the lowest interface area of all the human isotypes. The nature of the residues that form the dimer interface also differs from those conserved in the other isotypes. By contrast, the interface between the Cδ2 and Cδ3 domains in each chain is the largest among the human isotypes. This interface is characterized by two binding pockets, not seen in other isotypes, and points to a potential role for the Cδ2/Cδ3 interface in stabilizing the IgD-Fc homodimer. We investigated the thermal stability of IgD-Fc, alone and in the context of an intact IgD antibody, and found that IgD-Fc unfolds in a single transition. Human IgD-Fc clearly has unique structural features not seen in the other human isotypes, and comparison with other mammalian IgD sequences suggests that these unique features might be widely conserved.</p>","PeriodicalId":56271,"journal":{"name":"Proteins-Structure Function and Bioinformatics","volume":" ","pages":"786-800"},"PeriodicalIF":3.2,"publicationDate":"2025-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11878202/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142711704","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":"PCANN Program for Structure-Based Prediction of Protein-Protein Binding Affinity: Comparison With Other Neural-Network Predictors.","authors":"Olga O Lebedenko, Mikhail S Polovinkin, Anastasiia A Kazovskaia, Nikolai R Skrynnikov","doi":"10.1002/prot.26821","DOIUrl":"https://doi.org/10.1002/prot.26821","url":null,"abstract":"<p><p>In this communication, we introduce a new structure-based affinity predictor for protein-protein complexes. This predictor, dubbed PCANN (Protein Complex Affinity by Neural Network), uses the ESM-2 language model to encode the information about protein binding interfaces and graph attention network (GAT) to parlay this information into <math> <semantics> <mrow><msub><mi>K</mi> <mi>d</mi></msub> </mrow> <annotation>$$ {K}_{mathrm{d}} $$</annotation></semantics> </math> predictions. In the tests employing two previously unused literature-extracted datasets, PCANN performed better than the best of the publicly available predictors, BindPPI, with mean absolute error (MAE) of 1.3 versus 1.4 kcal/mol. Further progress in the development of <math> <semantics> <mrow><msub><mi>K</mi> <mi>d</mi></msub> </mrow> <annotation>$$ {K}_{mathrm{d}} $$</annotation></semantics> </math> predictors using deep learning models is faced with two problems: (i) the amount of experimental data available to train and test new predictors is limited and (ii) the available <math> <semantics> <mrow><msub><mi>K</mi> <mi>d</mi></msub> </mrow> <annotation>$$ {K}_{mathrm{d}} $$</annotation></semantics> </math> data are often not very accurate and lack internal consistency with respect to measurement conditions. These issues can be potentially addressed through an AI-leveraged literature search followed by careful human curation and by introducing additional parameters to account for variations in experimental conditions.</p>","PeriodicalId":56271,"journal":{"name":"Proteins-Structure Function and Bioinformatics","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-03-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143671758","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 Overview of Property, Design, and Functionality of Linkers for Fusion Protein Construction.","authors":"Hadis Chatrdooz, Javad Sargolzaei","doi":"10.1002/prot.26812","DOIUrl":"https://doi.org/10.1002/prot.26812","url":null,"abstract":"<p><p>Linkers are naturally occurring short amino acid sequences that are used to separate domains within a protein. The advent of recombinant DNA technology has made it possible to combine two interacting partners by introducing artificial linkers that often, allow for the production of stable and functional proteins. Glycine-rich linkers are useful for transient interactions, especially where the interaction is weak, by covalently linking proteins and forming a stable protein-protein complex. These linkers have also been used to generate covalently stable dimers and to connect two independent domains that create a ligand binding site or recognition sequence. Various structures of covalently linked protein complexes have been described using nuclear magnetic resonance methods, cryo-electron microscopy techniques, and X-ray crystallography; in addition, several structures where linkers have been used to generate stable protein-protein complexes, improve protein solubility, and obtain protein dimers are investigated, and also the design and engineering of the linker in fusion proteins is discussed. Therefore, one of the main factors for linker design and optimization is their flexibility, which can directly contribute to the physical distance between the domains of a fusion protein and describe the tendency of a linker to maintain a stable conformation during expression. We summarize the research on design and bioinformatics can be used to predict the spatial structure of the fusion protein. To perform simulations of spatial structures and drug molecule design, future research will concentrate on various correlation models.</p>","PeriodicalId":56271,"journal":{"name":"Proteins-Structure Function and Bioinformatics","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-03-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143659812","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":"Integrative Protein Assembly With LZerD and Deep Learning in CAPRI 47-55.","authors":"Charles Christoffer, Yuki Kagaya, Jacob Verburgt, Genki Terashi, Woong-Hee Shin, Anika Jain, Daipayan Sarkar, Tunde Aderinwale, Sai Raghavendra Maddhuri Venkata Subramaniya, Xiao Wang, Zicong Zhang, Yuanyuan Zhang, Daisuke Kihara","doi":"10.1002/prot.26818","DOIUrl":"https://doi.org/10.1002/prot.26818","url":null,"abstract":"<p><p>We report the performance of the protein complex prediction approaches of our group and their results in CAPRI Rounds 47-55, excluding the joint CASP Rounds 50 and 54, as well as the special COVID-19 Round 51. Our approaches integrated classical pipelines developed in our group as well as more recently developed deep learning pipelines. In the cases of human group prediction, we surveyed the literature to find information to integrate into the modeling, such as assayed interface residues. In addition to any literature information, generated complex models were selected by a rank aggregation of statistical scoring functions, by generative model confidence, or by expert inspection. In these CAPRI rounds, our human group successfully modeled eight interfaces and achieved the top quality level among the submissions for all of them, including two where no other group did. We note that components of our modeling pipelines have become increasingly unified within deep learning approaches. Finally, we discuss several case studies that illustrate successful and unsuccessful modeling using our approaches.</p>","PeriodicalId":56271,"journal":{"name":"Proteins-Structure Function and Bioinformatics","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-03-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143652274","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":"The Actin-Binding Prolyl-Isomerase Par17 Sustains Its Substrate Selectivity by Interdomain Allostery.","authors":"Anna Sternberg, Jennifer Lynne Borger, Mathilda Thies, Anja Matena, Mike Blueggel, Bianca E Kamba, Christine Beuck, Farnusch Kaschani, Markus Kaiser, Peter Bayer","doi":"10.1002/prot.26807","DOIUrl":"https://doi.org/10.1002/prot.26807","url":null,"abstract":"<p><p>The human peptidyl-prolyl-cis/trans isomerases (PPIases), Parvulin 14 and Parvulin 17, accelerate the cis/trans isomerization of Xaa-Pro moieties within protein sequences. By modulating the respective binding interfaces of their target proteins, they play a crucial role in determining the fate of their substrates within the cell. Although both enzymes share the same amino acid sequence, they have different cellular functions. This difference is due to a 25 residue N-terminal extension present in Par17 but absent in Par14. Using activity assays, NMR spectroscopy, and mass spectrometry, we demonstrate that the N-terminal extension of Par17 determines substrate selectivity by an intramolecular allosteric mechanism and exhibits a target-binding motif that interacts with actin.</p>","PeriodicalId":56271,"journal":{"name":"Proteins-Structure Function and Bioinformatics","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-03-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143607313","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":"Insights Into the Conformational Dynamics of the Cytoplasmic Domain of Metal-Sensing Sensor Histidine Kinase ZraS.","authors":"Nilima Mahapatra, Pranjal Mahanta, Shubhant Pandey, Rudresh Acharya","doi":"10.1002/prot.26819","DOIUrl":"https://doi.org/10.1002/prot.26819","url":null,"abstract":"<p><p>ZraS is a metal sensor integral to ZraPSR, a two-component signaling system found in enterobacters. It belongs to a family of bifunctional sensor histidine kinases (SHKs) and is speculated to sense zinc-induced stress on the bacterial envelope. Information on the structure-function relationship of sensor kinases is elusive due to the lack of full-length structures, intrinsically dynamic behavior, and difficulty trapping them in active state conformations. While the kinase domains (KDs) of a few SHKs are well characterized, they exhibit significant functional diversity attributed to their modular multi-domain arrangement in the cytoplasmic region, combined with other signal transducing elements such as simple helices, HAMP, and PAS domains. We report the crystal structure of the entire cytoplasmic region of Escherichia coli ZraS (EcZraS-CD) resolved at a resolution of 2.49 Å, comprising a unique helical linker and the KD. In the asymmetric unit, four molecules of ZraS assemble as homodimers trapped as two ligand-bound occluded conformers. Our analysis using these conformers shows that modulation of the dimer bundle through segmental helical bending, sliding, and rotation leads to the reorganization of the dimerization interface during kinase activation. Further, our analysis reveals the significance of aromatic amino acid interactions and loop residues at the dimer base in regulating the directionality of rotation during autophosphorylation. We also performed an in vitro coupled assay to determine ATPase activity. Overall, our findings provide structure-based mechanistic insights into the process of autophosphorylation in trans-acting SHKs.</p>","PeriodicalId":56271,"journal":{"name":"Proteins-Structure Function and Bioinformatics","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-03-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143588007","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":"Investigating Local Sequence-Structural Attributes of Amyloidogenic Light Chain Variable Domains.","authors":"Puneet Rawat, R Prabakaran, Divya Sharma, Vasanth Mandala, Victor Greiff, Sandeep Kumar, M Michael Gromiha","doi":"10.1002/prot.26815","DOIUrl":"https://doi.org/10.1002/prot.26815","url":null,"abstract":"<p><p>Light chain amyloidosis is a medical condition characterized by the aggregation of misfolded antibody light chains into insoluble amyloid fibrils in the target organs, causing organ dysfunction, organ failure, and death. Despite extensive research to understand the factors contributing to amyloidogenesis, accurately predicting whether a given protein will form amyloids under specific conditions remains a formidable challenge. In this study, we have conducted a comprehensive analysis to understand the amyloidogenic tendencies within a dataset containing 1828 (348 amyloidogenic and 1480 non-amyloidogenic) antibody light chain variable region (V_L) sequences obtained from the AL-Base database. Physicochemical and structural features often associated with protein aggregation, such as net charge, isoelectric point (pI), and solvent-exposed hydrophobic regions did not reveal a consistent association with the aggregation capability of the antibody light chains. However, the solvent-exposed aggregation-prone regions (APRs) occur with higher frequencies among the amyloidogenic light chains when compared with the non-amyloidogenic ones, with the difference ranging from 2% to 15% at various relative solvent-accessible surface area (rASA) cutoffs. We have, for the first time, identified structural gatekeeping residues around the APRs and assessed their impact on the amyloidogenicity of the antibody light chains. The non-amyloidogenic light chains contain these structural gatekeeper residues vicinal to their APRs more often than the amyloidogenic ones. We observed that the rASA cutoff of 35% is optimal for identifying the surface-exposed APRs, and a 4 Å distance cutoff from the APR motif(s) is optimal for identifying the structural gatekeeper residues. Moreover, lambda light chains were found to contain solvent-exposed APRs more often and surrounded by fewer gatekeepers, rendering them more susceptible to aggregation. The insights gained from this report have significant implications for understanding the molecular origins of light-chain amyloidosis in humans and the design of aggregation-resistant therapeutic antibodies.</p>","PeriodicalId":56271,"journal":{"name":"Proteins-Structure Function and Bioinformatics","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-03-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143544682","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":"Understanding the Role of RING-Between-RING E3 Ligase of the Human Malaria Parasite.","authors":"Varsha Kumari, Seema Vidyarthi, Aradhya Tripathi, Nirupa Chaurasia, Niharika Rai, Richa Shukla, Shagufa Nisrat Noorie, Girdhar Bhati, Simmi Anjum, Mohammad Anas, Shakil Ahmed, Niti Kumar","doi":"10.1002/prot.26813","DOIUrl":"https://doi.org/10.1002/prot.26813","url":null,"abstract":"<p><p>E3 ligases constitute an important component of proteostasis machinery, which plays a critical role in the survival of malaria parasites through post-translational modifications of their protein substrates. In contrast to humans, parasite E3 ligases have not been extensively studied. Here, we characterize a unique Plasmodium E3 ligase that has both RING and HECT-like features with zinc-coordinating domains. Plasmodium encodes a single RING-between-RING (RBR) E3 ligase that has evolutionarily diverged from human and other intracellular parasites. This RBR-E3 ligase is expressed throughout the erythrocytic phase of the P. falciparum lifecycle. Immunoprecipitation experiments showed that Pf RBR-E3 ligase catalyzes K6, K11, K48, and K63 mediated polyubiquitination, hinting towards its probable biological roles (DNA repair, proteasomal degradation, mitochondrial quality control). We observed that Pf RBR-E3 ligase interacts with UBCH5 and UBC13 family of E2-conjugating enzymes. Through mutational analysis in Pf RBR-E3 ligase, we identified residues in RING1 and RING2 domains that are critical for ubiquitination activity and its protein stability. Pf RBR-E3 ligase exhibits differences in immunofluorescence profile upon exposure of the parasite to different genotoxic (MMS) and proteotoxic (MG132, FCCP and artemisinin derivative) stress. Our study opens up avenues for exploring the client substrates of Pf RBR-E3 ligase and using this knowledge to design substrate-specific protein degradation-based alternative intervention strategies for malaria.</p>","PeriodicalId":56271,"journal":{"name":"Proteins-Structure Function and Bioinformatics","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-03-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143544641","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}