Biochimica et biophysica acta. Biomembranes最新文献

{"title":"Effects induced by η6-p-cymene ruthenium(II) complexes on Langmuir monolayers mimicking cancer and healthy cell membranes do not correlate with their toxicity","authors":"Ellen C. Wrobel ,&nbsp;Ivelise Dimbarre Lao Guimarães ,&nbsp;Karen Wohnrath ,&nbsp;Osvaldo N. Oliveira Jr","doi":"10.1016/j.bbamem.2024.184332","DOIUrl":"10.1016/j.bbamem.2024.184332","url":null,"abstract":"<div><p>The mechanism of chemotherapeutic action of Ru-based drugs involves plasma membrane disruption and valuable insights into this process may be gained using cell membrane models. The interactions of a series of cytotoxic η⁶-<em>p</em>-cymene ruthenium(II) complexes, [Ru(η⁶-<em>p</em>-cymene)P(3,5-C(CH₃)₃-C₆H₃)₃Cl₂] <strong>(1)</strong>, [Ru(η⁶-<em>p</em>-cymene)P(3,5-CH₃-C₆H₃)₃Cl₂] <strong>(2)</strong>, [Ru(η⁶-<em>p</em>-cymene)P(4-CH₃O-3,5-CH₃-C₆H₂)₃Cl₂] <strong>(3)</strong>, and [Ru(η⁶-<em>p</em>-cymene)P(4-CH₃O-C₆H₄)₃Cl₂] <strong>(4)</strong>, were examined using Langmuir monolayers as simplified healthy and cancerous outer leaflet plasma membrane models. The cancerous membrane (CM1 and CM2) models contained either 40 % 1,2- dipalmitoyl-<em>sn</em>-glycero-3-phosphocholine (DPPC) or 1,2-dioleoyl-<em>sn</em>-glycero-3-phosphocholine (DOPC), 30 % cholesterol (Chol), 20 % 1,2-dipalmitoyl-<em>sn</em>-glycero-3-phosphoethanolamine (DPPE), and 10 % 1,2-dipalmitoyl-<em>sn</em>-glycero-3-phospho-<em><span>l</span></em>-serine (DPPS). Meanwhile, the healthy membrane (HM1 and HM2) models were composed of 60 % DPPC or DOPC, 30 % Chol and 10 % DPPE. The complexes affected surface pressure isotherms and decreased compressional moduli of cancerous and healthy membrane models, interacting with the monolayers headgroup and tails according to data from polarization-modulated infrared reflection absorption spectroscopy (PM-IRRAS). However, the effects did not correlate with the toxicity of the complexes to cancerous and healthy cells. Multidimensional projection technique showed that the complex <strong>(1)</strong> induced significant changes in the CM1 and HM1 monolayers, though it had the lowest cytotoxicity against cancer cells and is not toxic to healthy cells. Moreover, the most toxic complexes <strong>(2)</strong> and <strong>(4)</strong> were those that least affected CM2 and HM2 monolayers. The findings here support that the ruthenium complexes interact with lipids and cholesterol in cell membrane models, and their cytotoxic activities involve a multifaceted mode of action beyond membrane disruption.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 5","pages":"Article 184332"},"PeriodicalIF":3.4,"publicationDate":"2024-05-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140916013","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":"Helical reorganization in the context of membrane protein folding: Insights from simulations with bacteriorhodopsin (BR) fragments","authors":"Hindol Chatterjee ,&nbsp;Anshuman J. Mahapatra ,&nbsp;Martin Zacharias ,&nbsp;Neelanjana Sengupta","doi":"10.1016/j.bbamem.2024.184333","DOIUrl":"10.1016/j.bbamem.2024.184333","url":null,"abstract":"<div><p>Membrane protein folding is distinct from folding of soluble proteins. Conformational acquisition in major membrane protein subclasses can be delineated into insertion and folding processes. An exception to the “two stage” folding, later developed to “three stage” folding, is observed within the last two helices in bacteriorhodopsin (BR), a system that serves as a model membrane protein. We employ a reductionist approach to understand interplay of molecular factors underlying the apparent defiance. Leveraging available solution NMR structures, we construct, sample in silico, and analyze partially (PIn) and fully inserted (FIn) BR membrane states. The membrane lateral C-terminal helix (CH) in PIn is markedly prone to transient structural distortions over microsecond timescales; a disorder prone region (DPR) is thereby identified. While clear transmembrane propensities are not acquired, the distortions induce alterations in local membrane curvature and area per lipid. Importantly, energetic decompositions reveal that overall, the N-terminal helix (NH) is thermodynamically more stable in the PIn. Higher overall stability of the FIn arises from favorable interactions between the NH and the CH. Our results establish lack of spontaneous transition of the PIn to the FIn, and attributes their partitioning to barriers that exceed those accessible with thermal fluctuations. This work paves the way for further detailed studies aimed at determining the thermo-kinetic roles of the initial five helices, or complementary external factors, in complete helical folding and insertion in BR. We comment that complementing such efforts with the growing field of machine learning assisted energy landscape searches may offer unprecedented insights.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 5","pages":"Article 184333"},"PeriodicalIF":3.4,"publicationDate":"2024-05-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140916020","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":"Exogenous polyserine fibrils change membrane properties of phosphatidylcholine-liposome and red blood cells","authors":"Yutaro Iizuka ,&nbsp;Akiko Katano-Toki ,&nbsp;Fumio Hayashi ,&nbsp;Jun Fujioka ,&nbsp;Hiroshi Takahashi ,&nbsp;Kazuhiro Nakamura","doi":"10.1016/j.bbamem.2024.184331","DOIUrl":"10.1016/j.bbamem.2024.184331","url":null,"abstract":"<div><p>The causative genes for neurodegenerative polyglutamine (polyQ) diseases produce homopolymeric polyglutamine (polyQ), polyserine (polyS), polyalanine (polyA), polycysteine (polyC), and polyleucine (polyL) sequences by repeat-associated non-AUG (RAN) translation. The cytotoxicity of the intracellular polyQ and RAN products has been extensively investigated. However, little is known about the toxicity of the extracellular polyQ and RAN products on the membranes of viable cells. Because polyQ aggregates induce a deflated morphology of a model membrane, we hypothesized that extracellular polyQ and RAN products might affect the membrane properties of viable cells. In this study, we demonstrated that exogenous polyS fibrils but not polyS or polyQ non-fibril aggregates altered the thermal phase transition behavior of a model membrane composed of a phosphatidylcholine bilayer using differential scanning calorimetry. PolyS fibrils induced morphological changes in viable red blood cells (RBCs). However, both polyS and polyQ non-fibril aggregates had no effects on RBCs. These results highlight the possibility that extracellular fibrils generated from RAN products may alter the properties of neuronal cell membranes, which may contribute to changes in the brain pathology.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 5","pages":"Article 184331"},"PeriodicalIF":3.4,"publicationDate":"2024-05-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140891372","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":"Notable enhancement of Amphotericin B channel activity by applied pressures in the range of MS channel activation","authors":"Tammy Haro-Reyes,&nbsp;Iván Ortega-Blake","doi":"10.1016/j.bbamem.2024.184326","DOIUrl":"https://doi.org/10.1016/j.bbamem.2024.184326","url":null,"abstract":"<div><p>The mechanism of Amphotericin B at the membrane is still subject of debate, with the prevailing hypothesis being the formation of pores. The activity of these pores is influenced by various factors. Recently aggregation in solution and insertion in the membrane had been highlighted as crucial for action of the drug</p><p>Here we investigated the effect of applied pressure on the activity of Amphotericin B. Our findings demonstrate that applied pressure of 50 mmHg is sufficient to enhance the activity.</p><p>We interpreted the results as supporting the idea that pressure fractures the membrane and promotes the insertion of the polyene</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 5","pages":"Article 184326"},"PeriodicalIF":3.4,"publicationDate":"2024-05-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140823972","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":"The molecular arrangement of ceramides in the unit cell of the long periodicity phase of stratum corneum models shows a high adaptability to different ceramide head group structures","authors":"Andreea Nădăban ,&nbsp;Gerrit S. Gooris ,&nbsp;Charlotte M. Beddoes ,&nbsp;Robert M. Dalgliesh ,&nbsp;Marc Malfois ,&nbsp;Bruno Demé ,&nbsp;Joke A. Bouwstra","doi":"10.1016/j.bbamem.2024.184324","DOIUrl":"https://doi.org/10.1016/j.bbamem.2024.184324","url":null,"abstract":"<div><p>The stratum corneum (SC) lipid matrix, composed primarily of ceramides (CERs), cholesterol and free fatty acids (FFA), has an important role for the skin barrier function. The presence of the long periodicity phase (LPP), a unique lamellar phase, is characteristic for the SC. Insight into the lipid molecular arrangement within the LPP unit cell is imperative for understanding the relationship between the lipid subclasses and the skin barrier function. In this study, the impact of the CER head group structure on the lipid arrangement and barrier functionality was investigated using lipid models forming the LPP. The results demonstrate that the positions of CER <em>N</em>-(tetracosanoyl)-sphingosine (CER NS) and CER <em>N</em>-(tetracosanoyl)-phytosphingosine (CER NP), two essentials CER subclasses, are not influenced by the addition of another CER subclass (<em>N</em>-(tetracosanoyl)-dihydrosphingosine (CER NdS), <em>N</em>-(2R-hydroxy-tetracosanoyl)-sphingosine (CER AS) or D-(2R-hydroxy-tetracosanoyl)-phytosphingosine (CER AP)). However, differences are observed in the lipid organization and the hydrogen bonding network of the three different models. A similar localization of CER NP and CER NS is also observed in a more complex lipid model, with the CER subclass composition mimicking that of human SC. These studies show the adaptability and insensitivity of the LPP unit cell structure to changes in the lipid head group structures of the CER subclasses.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 5","pages":"Article 184324"},"PeriodicalIF":3.4,"publicationDate":"2024-04-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0005273624000555/pdfft?md5=413b5cd0ac026b81be015cbcfba400f5&pid=1-s2.0-S0005273624000555-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140823970","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":"Interaction of L-phenylalanine with carbonyl groups in mixed lipid membranes","authors":"María A. Brandan,&nbsp;Hugo A. Pérez,&nbsp;Aníbal Disalvo,&nbsp;María de los A. Frías","doi":"10.1016/j.bbamem.2024.184328","DOIUrl":"10.1016/j.bbamem.2024.184328","url":null,"abstract":"<div><p>The interaction of L-Phe with the membrane components, <em>i.e.</em>, lipids and proteins, has been discussed in the current literature due to the interest to understand the effect of single amino acids in relation to the formation of amyloid aggregates.</p><p>In the present work, it is shown that L-Phe interacts with 9:1 DMPC (1,2-dimyristoyl-<em>sn</em>-glycero-3 phosphocholine)/DPPC (1,2-dipalmitoyl-<em>sn</em>-glycero-3 phosphocholine) mixtures but not in the 1:9 one. An important observation is that the interaction disappears when DPPC is replaced by diether PC (2-di-<em>O</em>-hexadecyl-<em>sn</em>-glycero-3-phosphocholine) a lipid lacking carbonyl groups (CO). This denotes that CO groups may interact specifically with L-Phe in accordance with the appearance of a new peak observed by Infrared spectroscopy (FTIR-ATR). The interaction of L-Phe affects the compressibility pattern of the 9:1 DMPC/DPPC mixture which is congruent with the changes observed by Raman spectra.</p><p>The specific interaction of L-Phe with CO, propagates to phosphate and choline groups in this particular mixture as analyzed by FTIR-ATR spectroscopy and is absent when DMPC is dopped with diether PC.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 5","pages":"Article 184328"},"PeriodicalIF":3.4,"publicationDate":"2024-04-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140855849","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":"Insights into short chain polyethylene penetration of phospholipid bilayers via atomistic molecular dynamics simulations","authors":"Franciszek Włodek ,&nbsp;Waldemar Kulig ,&nbsp;Anna Stachowicz-Kuśnierz","doi":"10.1016/j.bbamem.2024.184327","DOIUrl":"https://doi.org/10.1016/j.bbamem.2024.184327","url":null,"abstract":"<div><p>The escalation of global plastic production, reaching an annual output of 400 million tons, has significantly intensified concerns regarding plastic waste management. This has been exacerbated by improper recycling and disposal practices, contributing to the impending crisis of plastic pollution. Predictions indicate that by 2025, the environment will bear the burden of over ten billion metric tons of accumulated plastic waste. This situation has led to the concerning release of microplastics and nanoplastics (NPs) into the environment as plastic materials degrade, thereby posing risks to both ecosystems and human health. Nanoparticle interactions with living organisms have garnered significant attention due to their potential to disrupt vital biological processes. Of particular interest are lipid membranes, acting as crucial gatekeepers, underscoring the importance of comprehending the intricate process of NP penetration. Molecular dynamics (MD) simulations serve as a robust tool, offering molecular-level insights into these intricate interactions. In this study, we leverage all-atom MD simulations to delve into the interactions between lipid bilayers and polyethylene (PETH) chains of varying lengths. The investigation spans diverse lipid bilayer compositions—ranging from pure POPC to POPC:DPPC mixtures—revealing how PETH accommodates itself, adopts extended conformations, and influences membrane structure and ordering. Significantly, while longer PETH chains demonstrate limited passive diffusion, their potential to penetrate bilayers over extended timescales emerges as a significant revelation. Overall, this research significantly advances our comprehension of NP-membrane interactions, shedding light on the potential environmental and health implications that lie ahead.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 5","pages":"Article 184327"},"PeriodicalIF":3.4,"publicationDate":"2024-04-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140823971","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":"Processes and mechanisms underlying burst of giant unilamellar vesicles induced by antimicrobial peptides and compounds","authors":"Md. Masum Billah ,&nbsp;Marzuk Ahmed ,&nbsp;Md. Zahidul Islam ,&nbsp;Masahito Yamazaki","doi":"10.1016/j.bbamem.2024.184330","DOIUrl":"https://doi.org/10.1016/j.bbamem.2024.184330","url":null,"abstract":"<div><p>To clarify the damage of lipid bilayer region in bacterial cell membrane caused by antimicrobial peptides (AMPs) and antimicrobial compounds (AMCs), their interactions with giant unilamellar vesicles (GUVs) of various lipid compositions have been examined. The findings revealed two main causes for the leakage: nanopore formation in the membrane and burst of GUVs. Although GUV burst has been explained previously based on the carpet model, the supporting evidence is limited. In this review, to better clarify the mechanism of GUV burst by AMPs, AMCs, and other membrane-active peptides, we described current knowledge of the conditions, characteristics, and detailed processes of GUV burst and the changes in the shape of the GUVs during burst. We identified several physical factors that affect GUV burst, such as membrane tension, electrostatic interaction, structural changes of GUV membrane such as membrane folding, and oil in the membrane. We also clarified one of the physical mechanisms underlying the instability of lipid bilayers that are associated with leakage in the carpet model. Based on these results, we propose a mechanism underlying some types of GUV burst induced by these substances: the growth of a nanopore to a micropore, resulting in GUV burst.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 5","pages":"Article 184330"},"PeriodicalIF":3.4,"publicationDate":"2024-04-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140823973","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":"Effect of VBIT-4 on the functional activity of isolated mitochondria and cell viability","authors":"Konstantin N. Belosludtsev ,&nbsp;Anna I. Ilzorkina ,&nbsp;Lyudmila A. Matveeva ,&nbsp;Alexander V. Chulkov ,&nbsp;Alena A. Semenova ,&nbsp;Mikhail V. Dubinin ,&nbsp;Natalia V. Belosludtseva","doi":"10.1016/j.bbamem.2024.184329","DOIUrl":"https://doi.org/10.1016/j.bbamem.2024.184329","url":null,"abstract":"<div><p>VBIT-4 is a new inhibitor of the oligomerization of VDAC proteins of the outer mitochondrial membrane preventing the development of oxidative stress, mitochondrial dysfunction, and cell death in various pathologies. However, as a VDAC inhibitor, VBIT-4 may itself cause mitochondrial dysfunction in healthy cells. The article examines the effect of VBIT-4 on the functional activity of rat liver mitochondria and cell cultures. We have demonstrated that high concentrations of VBIT-4 (15–30 μM) suppressed mitochondrial respiration in state 3 and 3U_DNP driven by substrates of complex I and II. VBIT-4 induced depolarization of organelles fueled by substrates of complex I but not complex II of the respiratory chain. VBIT-4 has been found to inhibit the activity of complexes I, III, and IV of the respiratory chain. Molecular docking demonstrated that VBIT-4 interacts with the rotenone-binding site in complex I with similar affinity. 15–30 μM VBIT-4 caused an increase in H₂O₂ production in mitochondria, decreased the Ca²⁺ retention capacity, but increased the time of Ca²⁺-dependent mitochondrial swelling. We have found that the incubation of breast adenocarcinoma (MCF-7) with 30 μM VBIT-4 for 48 h led to the decrease of the mitochondrial membrane potential, an increase in ROS production and death of MCF-7 cells. The mechanism of action of VBIT-4 on mitochondria and cells is discussed.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 5","pages":"Article 184329"},"PeriodicalIF":3.4,"publicationDate":"2024-04-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140824036","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":"Effects of stand-alone polar residue on membrane protein stability and structure","authors":"Yu-Chu Chang ,&nbsp;Zheng Cao ,&nbsp;Wai-Ting Chen ,&nbsp;Wei-Chun Huang","doi":"10.1016/j.bbamem.2024.184325","DOIUrl":"10.1016/j.bbamem.2024.184325","url":null,"abstract":"<div><p>Helical membrane proteins generally have a hydrophobic nature, with apolar side chains comprising the majority of the transmembrane (TM) helices. However, whenever polar side chains are present in the TM domain, they often exert a crucial role in structural interactions with other polar residues, such as TM helix associations and oligomerization. Moreover, polar residues in the TM region also often participate in protein functions, such as the Schiff base bonding between Lys residues and retinal in rhodopsin-like membrane proteins. Although many studies have focused on these functional polar residues, our understanding of stand-alone polar residues that are energetically unfavored in TM helixes is limited. Here, we adopted bacteriorhodopsin (bR) as a model system and systematically mutated 17 of its apolar Leu or Phe residues to polar Asn. Stability measurements of the resulting mutants revealed that all of these polar substitutions reduced bR stability to various extents, and the extent of destabilization of each mutant bR is also correlated to different structural factors, such as the relative accessible surface area and membrane depth of the mutation site. Structural analyses of these Asn residues revealed that they form sidechain-to-backbone hydrogen bonds that alleviate the unfavorable energetics in hydrophobic and apolar surroundings. Our results indicate that membrane proteins are able to accommodate certain stand-alone polar residues in the TM region without disrupting overall structures.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 5","pages":"Article 184325"},"PeriodicalIF":3.4,"publicationDate":"2024-04-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140776671","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}