Biochimica et biophysica acta. Biomembranes最新文献

{"title":"Phospholipid-functionalized gold electrode for cellular membrane interface studies - interactions between DMPC bilayer and human cystatin C","authors":"Paweł Niedziałkowski ,&nbsp;Przemysław Jurczak ,&nbsp;Marta Orlikowska ,&nbsp;Anna Wcisło ,&nbsp;Jacek Ryl ,&nbsp;Tadeusz Ossowski ,&nbsp;Paulina Czaplewska","doi":"10.1016/j.bbamem.2023.184266","DOIUrl":"10.1016/j.bbamem.2023.184266","url":null,"abstract":"<div><p><span>This work describes the electrochemical studies on the interactions between V57G mutant of human cystatin C<span><span> (hCC V57G) and membrane bilayer<span> immobilized on the surface of a gold electrode. The electrode was modified with 6-mercaptohexan-1-ol (MCH) and 1,2-dimyristoyl-sn-glycero-3-phosphocholine (DMPC). DMPC was used as a membrane mimetic for monitoring electrochemical changes resulting from the interactions between the functionalized electrode surface and human cystatin C. The interactions between the modified electrode and hCC V57G were investigated by cyclic voltammetry and </span></span>electrochemical impedance spectroscopy in a phosphate buffered saline (PBS) containing Fe(CN)</span></span>₆^3−/4- as a redox probe. The electrochemical measurements confirm that fabricated electrode is sensitive to hCC V57G at the concentration of 1 × 10⁻¹⁴ M. The incubation studies carried out at higher concentrations resulted in insignificant changes observed in cyclic voltammetry and electrochemical impedance spectroscopy measurements. The calculated values of surface coverage θ_R confirm that the electrode is equally covered at higher concentrations of hCC V57G. Measurements of wettability and surface free energy made it possible to determine the influence of individual structural elements of the modified gold electrode on its properties, and thus allowed to understand the nature of the interactions. Contact angle values confirmed the results obtained during electrochemical measurements, indicating the sensitivity of the electrode towards hCC V57G at the concentration of 1 × 10⁻¹⁴<span> M. In addition, the XPS spectra confirmed the successful anchoring of hCC V57G to the DMPC-functionalized surface.</span></p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-12-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139048292","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Classifying tetraspanins: A universal system for numbering residues and a proposal for naming structural motifs and subfamilies","authors":"Luke M. Broadbent,&nbsp;Alice J. Rothnie,&nbsp;John Simms,&nbsp;Roslyn M. Bill","doi":"10.1016/j.bbamem.2023.184265","DOIUrl":"10.1016/j.bbamem.2023.184265","url":null,"abstract":"<div><p><span><span>All tetraspanins have four transmembrane domains<span> (TMs). The large extracellular loop (LEL) that connects the third and fourth TMs contains multiple secondary structures together with the family's signature Cys-Cys-Gly motif. These intriguing membrane proteins are involved in diverse and incompletely understood cellular processes including </span></span>cell adhesion<span><span>, tissue differentiation, immune cell<span><span> maturation and host-parasite interactions. Here we present a classification system that accurately describes the position of each amino acid within its primary sequence based on both sequence and topological conservation of the TMs and LEL. This builds on the numbering systems that have been used in the G protein-coupled receptor (GPCR) field for nearly three decades and which have aided the understanding of GPCR structure/activity relationships and ligand interactions. The high-resolution structures of the tetraspanins </span>CD81, </span></span>CD9<span>, CD53 and Tspan15 were used to validate the structural relevance of our new tetraspanin classification system. Modelling of all tetraspanin LELs highlighted flexibility in LEL </span></span></span>disulfide bonding<span> across the family and suggests that the structural arrangement of tetraspanin LELs is more complex than previously thought. We therefore propose a new subfamily naming system that addresses this added complexity and facilitates the systematic classification of human tetraspanins, shedding light on all structural motifs within the family. We anticipate that our universal tetraspanin classification system will enable progress in defining how sequence and structure inform function.</span></p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-12-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139054425","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Tryptophan- and arginine-rich antimicrobial peptides: Anti-infectives with great potential","authors":"Suzana K. Straus","doi":"10.1016/j.bbamem.2023.184260","DOIUrl":"10.1016/j.bbamem.2023.184260","url":null,"abstract":"<div><p>With the increasing prevalence of multidrug resistant (MDR) bacteria, there is a need to design synthetic antimicrobial peptides<span><span><span> (AMPs) that are effective and selective for bacteria, i.e. non-toxic to mammalian cells. One design strategy, namely the use of tryptophan- and arginine-rich AMPs, is rooted in the study of natural AMPs that are composed mainly of these </span>amino acids, such as </span>lactoferricin, tritrpticin, and puroindoline. A number of important studies on these AMPs by the Vogel group are reviewed here. More recent work on W-/R-rich peptides is also presented. The examples show that these peptides represent anti-infectives with great potential.</span></p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-12-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138683033","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Protein S-palmitoylation is markedly inhibited by 4″-alkyl ether lipophilic derivatives of EGCG, the major green tea polyphenol: In vitro and in silico studies","authors":"Anupama Binoy ,&nbsp;Manan Kothari ,&nbsp;Revathy Sahadevan ,&nbsp;Sayan Poddar ,&nbsp;Parimal Kar ,&nbsp;Sushabhan Sadhukhan","doi":"10.1016/j.bbamem.2023.184264","DOIUrl":"10.1016/j.bbamem.2023.184264","url":null,"abstract":"<div><p><em>S</em><span><span>-palmitoylation is a dynamic lipid-based protein post-translational modification facilitated by a family of protein acyltransferases (PATs) commonly known as DHHC-PATs or DHHCs. It is the only </span>lipid modification that is reversible, and this very fact uniquely qualifies it for therapeutic interventions through the development of DHHC inhibitors. Herein, we report that 4″-alkyl ether lipophilic derivatives of EGCG can effectively inhibit protein </span><em>S</em>-palmitoylation <em>in vitro</em>. With the help of metabolic labeling followed by copper(I)-catalyzed azide-alkyne cycloaddition Click reaction, we demonstrate that 4″-C₁₄ EGCG and 4″-C₁₆ EGCG markedly inhibited <em>S-</em><span><span>palmitoylation in various </span>mammalian cells<span> including HEK 293T, HeLa, and MCF-7 using both in gel fluorescence as well as confocal microscopy. Further, these EGCG derivatives were able to attenuate the </span></span><em>S</em>-palmitoylation to the basal level in DHHC3-overexpressed cells, suggesting that they are plausibly targeting DHHCs. Confocal microscopy data qualitatively reflected spatial and temporal distribution of <em>S</em>-palmitoylated proteins in different sub-cellular compartments and the inhibitory effects of 4″-C₁₄ EGCG and 4″-C₁₆ EGCG were clearly observed in the native cellular environment. Our findings were further substantiated by <em>in silico</em><span> analysis which revealed promising binding affinity and interactions of 4″-C</span>₁₄ EGCG and 4″-C₁₆<span><span> EGCG with key amino acid residues present in the hydrophobic cleft of the DHHC20 </span>enzyme. We also demonstrated the successful inhibition of </span><em>S</em><span>-palmitoylation of GAPDH by 4″-C</span>₁₆ EGCG. Taken together, our <em>in vitro</em> and <em>in silico</em> data strongly suggest that 4″-C₁₄ EGCG and 4″-C₁₆ EGCG can act as potent inhibitors for <em>S</em>-palmitoylation and can be employed as a complementary tool to investigate <em>S</em>-palmitoylation.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138682971","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Thermodynamic study on hydrated bilayers of ether-linked phosphatidylcholines with terminal perfluorobutyl group","authors":"Masaya Miyazaki ,&nbsp;Chika Arisaka ,&nbsp;Ai Nakagawara ,&nbsp;Nanako Sasaki ,&nbsp;Hiroshi Takahashi ,&nbsp;Toshiyuki Takagi ,&nbsp;Hideki Amii ,&nbsp;Masashi Sonoyama","doi":"10.1016/j.bbamem.2023.184261","DOIUrl":"10.1016/j.bbamem.2023.184261","url":null,"abstract":"<div><p><span>Novel terminally perfluorobutyl group-containing ether-linked phosphatidylcholines with different alkyl chain lengths (di-</span><em>O</em>-F4-Cn-PCs, <em>n</em> = 14,16 and 18) were developed as possible materials for stable liposomes aiming at applications of structural and functional analyses of membrane proteins. Differential scanning calorimetric investigations of the thermotropic transition of hydrated di-<em>O</em><span>-F4-Cn-PC bilayers demonstrated that the transition temperature of every di-</span><em>O</em>-F4-Cn-PC decreases by ~20 °C compared to their corresponding non-fluorinated PCs, di-<em>O</em>-Cn-PCs. With the elongation of the hydrophobic chain, on the other hand, the transition enthalpy (ΔH) and entropy (ΔS) increased in a linear manner. Comparison of ΔH and ΔS values against the net hydrocarbon chain length between di-<em>O</em>-F4-Cn-PCs and di-<em>O</em>-Cn-PCs strongly suggests that in the thermotropic transition of the di-<em>O</em>-F4-Cn-PC membrane, the perfluorobutyl segments undergo very limited structural changes; therefore, the hydrocarbon segments are mainly responsible for the phase transition.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-12-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138692763","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"OCTN1 (SLC22A4) displays two different transport pathways for organic cations or zwitterions","authors":"Lorena Pochini ,&nbsp;Francesca Barone ,&nbsp;Lara Console ,&nbsp;Chiara Brunocilla ,&nbsp;Michele Galluccio ,&nbsp;Mariafrancesca Scalise ,&nbsp;Cesare Indiveri","doi":"10.1016/j.bbamem.2023.184263","DOIUrl":"10.1016/j.bbamem.2023.184263","url":null,"abstract":"<div><h3>Background</h3><p>OCTN1 belongs to the SLC22 family, which includes transporters for cationic, zwitterionic, and anionic substrates. OCTN1 function and role in cells are still poorly understood. Not only cations, such as TEA, but also zwitterions, such as carnitine and ergothioneine, figure among transported molecules.</p></div><div><h3>Methods</h3><p>In this work, we carried out transport assays measuring [¹⁴C]-TEA and [³H]-Carnitine in proteoliposomes reconstituted with the recombinant human OCTN1 in the presence of Na⁺ or other cations. The homology model of OCTN1 was built using the structure of OCT3 as a template for docking analysis.</p></div><div><h3>Results</h3><p>TEA and carnitine did not inhibit each other. Moreover, carnitine uptake was not affected by the presence of Na⁺ and TEBA, whereas TEA was strongly inhibited by both compounds. Computational data revealed that TEA, Na⁺, and carnitine can interact with E381 in the OCTN1 substrate site. Differently from TEA, in the presence of Na⁺, carnitine is still able to interact with the binding site via R469.</p></div><div><h3>Conclusions</h3><p>The lack of mutual inhibition of the two prototype substrates, the different effect of Na⁺ and TEBA on their transport reaction, together with the computational analysis supports the existence of two transport pathways for cations and zwitterions.</p></div><div><h3>General significance</h3><p>The results shed new light on the transport mechanisms of OCTN1, helping to get further insights into the structure/function relationships. The described results correlate well with previous and very recent findings on the polyspecificity of the OCT group of transporters belonging to the same family.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-12-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0005273623001451/pdfft?md5=e37a90ad1f4acc20ad2091e788cd3034&pid=1-s2.0-S0005273623001451-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138574815","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Bilayer tension-induced clustering of the UPR sensor IRE1","authors":"Md Zobayer Hossain,&nbsp;Wylie Stroberg","doi":"10.1016/j.bbamem.2023.184262","DOIUrl":"10.1016/j.bbamem.2023.184262","url":null,"abstract":"<div><p><span>The endoplasmic reticulum acts as a protein quality control center where a range of chaperones and foldases facilitates protein folding. </span>IRE1<span><span> is a sensory transmembrane protein that transduces signals of proteotoxic stress by forming clusters and activating a cellular program called the </span>unfolded protein response<span><span> (UPR). Recently, membrane thickness variation due to membrane compositional changes have been shown to drive IRE1 cluster formation, activating the UPR even in the absence of proteotoxic stress. Here, we demonstrate a direct relationship between bilayer tension and UPR activation based on IRE1 dimer stability. The stability of the IRE1 dimer in a (50%DOPC-50%POPC) membrane at different applied bilayer tensions was analyzed via molecular dynamics simulations. The potential of mean force for IRE1 </span>dimerization<span> predicts a higher concentration of IRE1 dimers for both tensed and compressed ER membranes. This study shows that IRE1 may be a mechanosensitive membrane protein and establishes a direct biophysical relationship between bilayer tension and UPR activation.</span></span></span></p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138561559","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Multimerization of the heptad repeat regions of the SARS-CoV 2 spike protein","authors":"Christopher Aisenbrey ,&nbsp;Burkhard Bechinger","doi":"10.1016/j.bbamem.2023.184259","DOIUrl":"10.1016/j.bbamem.2023.184259","url":null,"abstract":"<div><p><span>The heptad repeat 1 and 2 (HR1, HR2) regions in the spike protein of SARS-CoV 2 play a key role in the fusogenic mechanism of the virus with the host cell. During the fusion process they are thought to rearrange into an interdomain multimer. Functional fragments of the heptad repeat 1 and 2 regions in the spike protein of SARS-CoV 2 were chemically synthesized, labeled with nitrofurazone (NBD) and their interactions investigated by fluorescence spectroscopy. Steady state emission, </span>fluorescence quenching, anisotropy and lifetime measurements in combination with a fluorophore dilution scheme were used to dissect multimer formation of HR1 and HR2 in quantitative detail. In addition, the investigation of the multimers by homo-FRET (via anisotropy) and lifetime measurements reveals new insights into the mechanism of fluorophore-fluorophore interactions in biological samples.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-12-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138557162","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Engraulisin: A novel marine derived cell penetrating peptide with activity against drug resistant bacteria","authors":"Saurabh Saraswat,&nbsp;Archana Chugh","doi":"10.1016/j.bbamem.2023.184255","DOIUrl":"10.1016/j.bbamem.2023.184255","url":null,"abstract":"<div><p>Cell penetrating peptides<span> (CPP) with their intrinsic ability to penetrate plasma membranes facilitate intracellular uptake of various macromolecules. Although a substantial number of CPPs have been reported over the last three decades, the number is still inadequate when compared to the theoretically feasible peptides with similar physicochemical composition.</span></p><p>Marine organisms, due to their hostile environment, are an immense source of several high-valued therapeutically relevant peptides. Various marine derived antibacterial, antimycotic and anticancer peptides have demonstrated improved activity in comparison to peptides of terrestrial origin. While a significant number of marine bioactive peptides exist, cell penetrating peptides from marine organisms remain unravelled.</p><p>In this study, we report Engraulisin from <span><em>Engraulis</em><em> japonicus</em></span><span>, a computationally derived novel cell penetrating peptide of marine origin. Engraulisin manifest successful uptake in mammalian cells<span><span> at 5 μM concentration with negligible cytotoxicity observed through MTT assay. Analysis of its cellular uptake mechanism revealed significant inhibition at 4 °C suggesting </span>endocytosis<span> as the major route of cellular entry. Interestingly, the novel peptide also demonstrated selective antimicrobial activity against </span></span></span><em>Methicillin-resistant Staphylococcus aureus</em> (<em>MRSA</em><span>). Additionally, molecular dynamics simulation with POPC<span> and POPG bilayer system unveiled significance of positively charged residues in forming a stable membrane interaction. Engraulisin represents a novel marine-derived cell penetrating peptide which can be explored for cellular delivery of pharmaceutically relevant molecules.</span></span></p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-11-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138298298","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Accurate calculation of affinity changes to the close state of influenza A M2 transmembrane domain in response to subtle structural changes of adamantyl amines using free energy perturbation methods in different lipid bilayers","authors":"Kyriakos Georgiou ,&nbsp;Athina Konstantinidi ,&nbsp;Johanna Hutterer ,&nbsp;Kathrin Freudenberger ,&nbsp;Felix Kolarov ,&nbsp;George Lambrinidis ,&nbsp;Ioannis Stylianakis ,&nbsp;Margarita Stampelou ,&nbsp;Günter Gauglitz ,&nbsp;Antonios Kolocouris","doi":"10.1016/j.bbamem.2023.184258","DOIUrl":"10.1016/j.bbamem.2023.184258","url":null,"abstract":"<div><p><span>Experimental binding free energies of 27 adamantyl amines against the influenza M2(22-46) WT tetramer, in its closed form at pH 8, were measured by ITC<span> in DPC micelles. The measured </span></span><em>K</em>_d's range is ~44 while the antiviral potencies (IC₅₀) range is ~750 with a good correlation between binding free energies computed with <em>K</em>_d and IC₅₀ values (<em>r</em><span><span> = 0.76). We explored with MD simulations (ff19sb, CHARMM36m) the binding profile of complexes with strong, moderate and weak binders embedded in DMPC, DPPC, </span>POPC or a viral mimetic membrane and using different experimental starting structures of M2.</span></p><p><span>To predict accurately differences in binding free energy in response to subtle changes in the structure of the ligands, we performed 18 alchemical perturbative single topology FEP/MD NPT simulations (OPLS2005) using the BAR estimator (Desmond software) and 20 dual topology calculations TI/MD NVT simulations (ff19sb) using the MBAR estimator (Amber software) for adamantyl amines in complex with M2(22-46) WT in DMPC, DPPC, POPC. We observed that both methods with all lipids show a very good correlation between the experimental and calculated relative binding free energies (</span><em>r</em> = 0.77–0.87, mue = 0.36–0.92 kcal mol^-1<span>) with the highest performance achieved with TI/MBAR and lowest performance with FEP/BAR in DMPC bilayers. When antiviral potencies are used instead of the </span><em>K</em>_d values for computing the experimental binding free energies we obtained also good performance with both FEP/BAR (<em>r</em> = 0.83, mue = 0.75 kcal mol^-1) and TI/MBAR (<em>r</em> = 0.69, mue = 0.77 kcal mol^-1).</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-11-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138298297","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}