Biochimica et biophysica acta. Biomembranes最新文献

{"title":"The α1 integrin cytoplasmic tail interacts with phosphoinositides and interferes with Akt activation","authors":"Josephine Labus ,&nbsp;Kerstin Tang ,&nbsp;Petra Henklein ,&nbsp;Ulrike Krüger ,&nbsp;Andreas Hofmann ,&nbsp;Sylvia Hondke ,&nbsp;Kerstin Wöltje ,&nbsp;Christian Freund ,&nbsp;Lothar Lucka ,&nbsp;Kerstin Danker","doi":"10.1016/j.bbamem.2023.184257","DOIUrl":"10.1016/j.bbamem.2023.184257","url":null,"abstract":"<div><p><span>Integrin α</span>₁β₁<span><span> is an adhesion receptor that binds to collagen and laminin. It regulates </span>cell adhesion, cytoskeletal organization, and migration. The cytoplasmic tail of the α</span>₁<span> subunit consists of 15 amino acids and contains six positively charged lysine residues. In this study, we present evidence that the α</span>₁ integrin cytoplasmic tail (α₁<span>CT) directly associates with phosphoinositides, preferentially with phosphatidylinositol 3,4,5-trisphosphate (PI(3,4,5)P</span>₃). Since the association was disrupted by calcium, magnesium and phosphate ions, this interaction appears to be in ionic nature. Here, the peptide-lipid interaction was driven by the conserved KIGFFKR motif. The exchange of both two potential phospholipid-binding lysines for glycines in the KIGFFKR motif increased α₁β₁<span> integrin-specific adhesion and F-actin cytoskeleton formation compared to cells expressing the unmodified α</span>₁ subunit, whereas only mutation of the second lysine at position 1171 increased levels of constitutively active α₁β₁<span> integrins on the cell surface. In addition, enhanced focal adhesion<span> formation and increased phosphorylation of focal adhesion kinase, but decreased phosphorylation of AKT was observed in these cells. We conclude that the KIGFFKR motif, and in particular lysine1171 is involved in the dynamic regulation of α</span></span>₁β₁ integrin activity and that the interaction of α₁CT with phosphoinositides may contribute to this process.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138294487","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":"Spontaneous transfer of small peripheral peptides between supported lipid bilayer and giant unilamellar vesicles","authors":"Emanuela Efodili ,&nbsp;Ashlynn Knight ,&nbsp;Maryem Mirza ,&nbsp;Cedric Briones ,&nbsp;Il-Hyung Lee","doi":"10.1016/j.bbamem.2023.184256","DOIUrl":"10.1016/j.bbamem.2023.184256","url":null,"abstract":"<div><p><span>Vesicular trafficking facilitates material transport between membrane-bound organelles. Membrane protein cargos are trafficked for relocation, recycling, and degradation during various physiological processes. </span><em>In vitro</em><span> fusion studies utilized synthetic lipid membranes<span> to study the molecular mechanisms of vesicular trafficking and to develop synthetic materials mimicking the biological membrane trafficking. Various fusogenic conditions which can induce vesicular fusion have been used to establish synthetic systems that can mimic biological systems. Despite these efforts, the mechanisms underlying vesicular trafficking of membrane proteins remain limited and robust </span></span><em>in vitro</em> methods that can construct synthetic trafficking systems for membrane proteins between large membranes (&gt;1 μm²<span>) are unavailable. Here, we provide data to show the spontaneous transfer of small membrane-bound peptides (∼4 kD) between a supported lipid bilayer<span> (SLB) and giant unilamellar vesicles (GUVs). We found that the contact between the SLB and GUVs led to the occasional but notable transfer of membrane-bound peptides in a physiological saline buffer condition (pH 7.4, 150 mM NaCl). Quantitative and dynamic time-lapse analyses suggested that the observed exchange occurred through the formation of hemi-fusion stalks between the SLB and GUVs. Larger protein cargos with a size of ∼77 kD could not be transferred between the SLB and GUVs, suggesting that the larger-sized cargos limited diffusion across the hemi-fusion stalk, which was predicted to have a highly curved structure. Compositional study showed Ni-chelated lipid head group was the essential component catalyzing the process. Our system serves as an example synthetic platform that enables the investigation of small-peptide trafficking between synthetic membranes and reveals hemi-fused lipid bridge formation as a mechanism of peptide transfer.</span></span></p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138290202","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":"Study of the correlation between the structure of selected triester of phosphatidylcholine and their impact on physicochemical properties of model mammalian membranes","authors":"Marzena Mach ,&nbsp;Łukasz Płachta ,&nbsp;Paweł Wydro","doi":"10.1016/j.bbamem.2023.184254","DOIUrl":"10.1016/j.bbamem.2023.184254","url":null,"abstract":"<div><p>Cationic lipids are synthetic compounds of amphiphilic character used in Drug Delivery Systems (DDS), especially in gene therapy, as the carriers of genetic material. As it is known, the main limitation of the application of cationic lipids in DDS is their high cytotoxicity after <em>in vivo</em> administration and low bioactivity. This is probably related to not fully known the relationship between the lipid structure and its activity as well as the mechanism of lipofection or drug delivery. Therefore, in this work we determined the impact of a selected group of cationic lipids - triesters of phosphatidylcholine (Et-PCs) - differing in their hydrophobic structure on model mammalian membranes. In the research, as model systems, Langmuir monolayers and liposomes were applied. It was shown that the incorporation of Et-PCs into model mammalian membranes weakens interactions between lipids, causing the increase of fluidity, disordering degree and permeability of membrane. The destabilization of the membrane in this way can facilitate the entry of drugs, carried inside cationic liposomes, into the pathological cell. Moreover, the studies prove that the structure of the hydrophobic part of cationic lipids also affects the properties of lipid membranes.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0005273623001360/pdfft?md5=f2f41951959f60d43bfe7cf6da7060cd&pid=1-s2.0-S0005273623001360-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138290203","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":"A closer look at calcium-induced interactions between phosphatidylserine-(PS) doped liposomes and the structural effects caused by inclusion of gangliosides or polyethylene glycol- (PEG) modified lipids","authors":"Philipp Grad ,&nbsp;Katarina Edwards ,&nbsp;Lars Gedda ,&nbsp;Víctor Agmo Hernández","doi":"10.1016/j.bbamem.2023.184253","DOIUrl":"10.1016/j.bbamem.2023.184253","url":null,"abstract":"<div><p>The effects of polyethylene glycol- (PEG) modified lipids and gangliosides on the Ca²⁺ induced interaction between liposomes composed of palmitoyl-oleoyl phosphatidylethanolamine (POPE) and palmitoyl-oleoyl phosphatidylserine (POPS) was investigated at physiological ionic strength. Förster resonance energy transfer (FRET) studies complemented with dynamic light scattering (DLS) and cryo-transmission electron microscopy (Cryo-EM) show that naked liposomes tend to adhere, rupture, and collapse on each other's surfaces upon addition of Ca²⁺, eventually resulting in the formation of large multilamellar aggregates and bilayer sheets. Noteworthy, the presence of gangliosides or PEGylated lipids does not prevent the adhesion-rupture process, but leads to the formation of small, long-lived bilayer fragments/disks. PEGylated lipids seem to be more effective than gangliosides at stabilizing these structures. Attractive interactions arising from ion correlation are proposed to be a driving force for the liposome-liposome adhesion and rupture processes. The results suggest that, in contrast with the conclusions drawn from previous solely FRET-based studies, direct liposome-liposome fusion is not the dominating process triggered by Ca²⁺ in the systems studied.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-11-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0005273623001359/pdfft?md5=2e98d4270514c416801ca7a8e16dd516&pid=1-s2.0-S0005273623001359-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138046135","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":"Solid-state NMR spectroscopy for structural studies of polypeptides and lipids in extended physiological membranes","authors":"Ahmad Saad ,&nbsp;Burkhard Bechinger","doi":"10.1016/j.bbamem.2023.184162","DOIUrl":"10.1016/j.bbamem.2023.184162","url":null,"abstract":"<div><p><span><span>Solid-state NMR is a quickly developing technique that allows one to obtain structural information at atomic resolution in extended lipid bilayers in a rather unique manner. Two approaches have been developed for membrane proteins and peptides namely </span>magic angle sample spinning and the use of uniaxially oriented membrane samples. The state-of-the-art of both approaches will be introduced and the perspectives of solid-state </span>NMR spectroscopy in the context of other structural biology techniques, pressing biomedical questions and membrane biophysics will be discussed.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-11-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"72208235","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":"Measuring the bending rigidity of microbial glucolipid (biosurfactant) bioamphiphile self-assembled structures by neutron spin-echo (NSE): Interdigitated vesicles, lamellae and fibers","authors":"Niki Baccile ,&nbsp;Vincent Chaleix ,&nbsp;Ingo Hoffmann","doi":"10.1016/j.bbamem.2023.184243","DOIUrl":"https://doi.org/10.1016/j.bbamem.2023.184243","url":null,"abstract":"<div><p>Bending rigidity, <em>k</em><span><span><span><span>, is classically measured for lipid membranes<span> to characterize their nanoscale mechanical properties as a function of composition. Widely employed as a comparative tool, it helps understanding the relationship between the lipid's molecular structure and the elastic properties of its corresponding </span></span>bilayer<span>. Widely measured for phospholipid membranes in the shape of giant unilamellar vesicles (GUVs), bending rigidity is determined here for three self-assembled structures formed by a new biobased glucolipid bioamphiphile, rather associated to the family of </span></span>glycolipid biosurfactants than </span>phospholipids. In its oleyl form, glucolipid G-C18:1 can assemble into vesicles or crystalline fibers, while in its stearyl form, glucolipid G-C18:0 can assemble into lamellar gels. Neutron spin-echo (NSE) is employed in the </span><em>q</em>-range between 0.3 nm⁻¹ (21 nm) and 1.5 nm⁻¹ (4.1 nm) with a spin-echo time in the range of up to 500 ns to characterize the bending rigidity of three different structures (Vesicle suspension, Lamellar gel, Fiber gel) solely composed of a single glucolipid. The low (<em>k</em> = 0.30 ± 0.04 <em>k</em>_<em>b</em><em>T</em>) values found for the Vesicle suspension and high values found for the Lamellar gel (<em>k</em> = 130 ± 40 <em>k</em>_<em>b</em><em>T</em>) and Fiber gel (<em>k</em> = 900 ± 500 <em>k</em>_<em>b</em><em>T</em>) are unusual when compared to most phospholipid membranes. By attempting to quantify for the first time the bending rigidity of self-assembled bioamphiphiles, this work not only contributes to the fundamental understanding of these new molecular systems, but it also opens new perspectives in their integration in the field of soft materials.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-10-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"92039333","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":"Lipid composition and properties affect protein-mediated carotenoid uptake efficiency from membranes","authors":"Kristina Likkei ,&nbsp;Marcus Moldenhauer ,&nbsp;Neslihan N. Tavraz ,&nbsp;Eugene G. Maksimov ,&nbsp;Nikolai N. Sluchanko ,&nbsp;Thomas Friedrich","doi":"10.1016/j.bbamem.2023.184241","DOIUrl":"10.1016/j.bbamem.2023.184241","url":null,"abstract":"<div><p><span><span>Carotenoids<span> are pigments of diverse functions ranging from coloration over light-harvesting to photoprotection. Yet, the number of carotenoid-binding proteins, which mobilize these pigments in physiological media, is limited, and the mechanisms of carotenoid mobilization are still not well understood. The same applies for the determinants of carotenoid uptake from membranes into carotenoproteins, especially regarding the dependence on the chemical properties of membrane lipids. Here, we investigate </span></span>xanthophyll uptake capacity and kinetics of a paradigmatic carotenoid-binding protein, the homolog of the Orange Carotenoid Protein's C-terminal domain from </span><span><em>Anabaena</em></span><span><span><span> sp. PCC 7120 (AnaCTDH), using liposomes formed from defined lipid species and loaded with </span>canthaxanthin (CAN) and echinenone (ECN), respectively. </span>Phospholipids<span><span> with different chain length and degree of saturation were investigated. The composition of carotenoid-loaded liposomes directly affected the incorporation yield and storage ratio of CAN and ECN as well as the rate of carotenoid uptake by AnaCTDH. Generally, saturated PC lipids were identified as unsuitable, and a high phase transition temperature of the lipids negatively affected the carotenoid incorporation and storage yield. For efficient carotenoid transfer, the velocity increases with increasing chain length or membrane thickness. An average transfer yield of 93 % and 43 % were obtained for the formation of AnaCTDH(CAN) and AnaCTDH(ECN) </span>holoproteins<span>, respectively. In summary, the most suitable lipids for the formation of AnaCTDH(CAN/ECN) holoproteins by carotenoid transfer from artificial liposomes are phosphatidylcholine (18:1) and phosphatidylglycerol (14:0). Thus, these two lipids provide the best conditions for further investigation of lipid-protein interaction and the carotenoid uptake process.</span></span></span></p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"49688545","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":"Simulations of naïve and KLA-activated macrophage plasma membrane models","authors":"Yueqi Niu ,&nbsp;Si Jia Chen ,&nbsp;Jeffery B. Klauda","doi":"10.1016/j.bbamem.2023.184242","DOIUrl":"10.1016/j.bbamem.2023.184242","url":null,"abstract":"<div><p>Macrophages (MAs), which play vital roles in human immune responses and lipid metabolisms, are implicated in the development and progression of atherosclerosis, a major contributor to cardiovascular diseases. Specifically, the abnormal lipid metabolism of oxidized low-density lipids (oxLDLs) in MAs is believed to be a crucial factor. However, the precise mechanism by which the MA membrane contributes to this altered lipid metabolism remains unclear. Lipidomic studies have revealed significant differences in membrane composition between various MA phenotypes. This study serves to provide and characterize complex realistic computational models for naïve (M0) and Kdo2-lipid A-activated (M1) state MA. Analyses of surface area per lipid (SA/lip), area compressibility modulus (<em>K</em>_A), carbon‑hydrogen order parameter (S_CH), electron density profile (EDP), tilt angles, two-dimension radial distribution functions (2D RDFs), mean squared displacement (MSD), hydrogen bonds (H-bonds), lipid clustering, and lipid wobble were conducted for both models. Results indicate that the M1 state MA membrane is more tightly packed, with increased chain order across lipid species, and forms PSM-DOPG-CHOL and PSM-SLPC-CHOL clusters. Importantly, the bilayer thicknesses reported for the models are in good agreement with experimental data for the thicknesses of transmembrane regions for MA integral proteins. These findings validate the described models as physiologically accurate for future computational studies of MA membranes and their residing proteins.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"49688546","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":"Factors influencing the detergent-free membrane protein isolation using synthetic nanodisc-forming polymers","authors":"Bankala Krishnarjuna ,&nbsp;Gaurav Sharma ,&nbsp;Thirupathi Ravula ,&nbsp;Ayyalusamy Ramamoorthy","doi":"10.1016/j.bbamem.2023.184240","DOIUrl":"10.1016/j.bbamem.2023.184240","url":null,"abstract":"<div><p>The detergent-free isolation of membrane proteins using synthetic polymers is becoming the desired approach for functional and structural studies of membrane proteins. Since the expression levels for many membrane proteins are low and a high yield of functionalized reconstituted membrane proteins is essential for <em>in vitro</em><span> studies, it is crucial to optimize the experimental conditions for a given polymer to solubilize target membranes/proteins effectively. The factors that affect membrane solubilization and subsequently the isolation of a target membrane protein include polymer concentration, polymer charge, temperature, pH, and concentration of divalent metal ions. Therefore, it is important to have knowledge about the efficacy of different types of polymers in solubilizing cell membranes. In this study, we evaluate the efficacy of inulin-based non-ionic polymers in solubilizing </span><em>E. coli</em><span> membranes enriched with rat flavin mononucleotide binding-domain (FBD) of cytochrome-P450-reductase (CPR) and rabbit cytochrome-b5 (Cyt-b5) under various solubilization conditions. Our results show that a 1:1 (w/w) membrane:polymer ratio, low temperature, high pH and sub-millimolar concentration of metal ions favor the solubilization of </span><em>E. coli</em> membranes enriched with FBD or Cyt-b5. Conversely, the presence of excess divalent metal ions affected the final protein levels in the polymer-solubilized samples. We believe that the results from this study provide knowledge to assess and plan the use of non-ionic polymers in membrane protein studies.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-10-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"49688544","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 effect of lipid composition on the thermal stability of nanodiscs","authors":"Tim G.J. Knetsch,&nbsp;Marcellus Ubbink","doi":"10.1016/j.bbamem.2023.184239","DOIUrl":"10.1016/j.bbamem.2023.184239","url":null,"abstract":"<div><p>Discoidal lipid nanoparticles (LNPs) called Nanodiscs (NDs) are derived from human high-density lipoprotein (HDL). Such biomimetics are ideally suited for the stabilization and delivery of pharmaceuticals, including chemicals, bio-active proteins and vaccines. The stability and circulation lifetimes of reconstituted HDL nanoparticles, including NDs, are variable. Lipids found in thermophilic archaea and bacteria are prime candidates for the stabilization of LNPs. We report the thermal stability of NDs prepared with lipids that differ in saturation, have either ether- or ester linkages between the fatty acid and glycerol backbone or contain isoprenoid fatty acid tails (phytanyl lipids). NDs with two saturated fatty acids show a much greater long-term thermostability than NDs with an unsaturated fatty acid. Ether fatty acid linkages, commonly found in thermophiles, did not improve stability of NDs compared to ester fatty acid linkages when using saturated lipids. NDs containing phytanyl and saturated alkyl fatty acids show similar stability at 37 °C. NDs assembled with phytanyl lipids contain three copies of the membrane scaffolding protein as opposed to the canonical dimer found in conventional NDs. The findings present a strong basis for the production of thermostable NDs through the selection of appropriate lipids and are likely broadly applicable to LNP development.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2023-10-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0005273623001219/pdfft?md5=7bc9ea70847365bbf126c736c97996e9&pid=1-s2.0-S0005273623001219-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"49688547","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}