{"title":"Recognition and remodeling of endosomal zones by sorting nexins","authors":"Michael Overduin, Rakesh Bhat","doi":"10.1016/j.bbamem.2024.184305","DOIUrl":"10.1016/j.bbamem.2024.184305","url":null,"abstract":"<div><p>The proteolipid code determines how cytosolic proteins find and remodel membrane surfaces. Here, we investigate how this process works with sorting nexins Snx1 and Snx3. Both proteins form sorting machines by recognizing membrane zones enriched in phosphatidylinositol 3-phosphate (PI3P), phosphatidylserine (PS) and cholesterol. This co-localized combination forms a unique “lipid codon” or lipidon that we propose is responsible for endosomal targeting, as revealed by structures and interactions of their PX domain-based readers. We outline a membrane recognition and remodeling mechanism for Snx1 and Snx3 involving this code element alongside transmembrane pH gradients, dipole moment-guided docking and specific protein-protein interactions. This generates an initial membrane-protein assembly (memtein) that then recruits retromer and additional PX proteins to recruit cell surface receptors for sorting to the <em>trans</em>-Golgi network (TGN), lysosome and plasma membranes. Post-translational modification (PTM) networks appear to regulate how the sorting machines form and operate at each level. The commonalities and differences between these sorting nexins show how the proteolipid code orchestrates parallel flows of molecular information from ribosome emergence to organelle genesis, and illuminates a universally applicable model of the membrane.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 4","pages":"Article 184305"},"PeriodicalIF":3.4,"publicationDate":"2024-02-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139970861","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}
V. Brandejsky , O. Leinhard Dahlqvist , E. Lund , P. Lundberg
{"title":"Phosphorus-31: A table-top method for 3D B1-field amplitude and phase measurements","authors":"V. Brandejsky , O. Leinhard Dahlqvist , E. Lund , P. Lundberg","doi":"10.1016/j.bbamem.2024.184307","DOIUrl":"10.1016/j.bbamem.2024.184307","url":null,"abstract":"<div><p>A novel method of high-spatial-resolution, 3D B<sub>1</sub>-field distribution measurements is presented. The method is independent of the MR-scanner, and it allows for automated acquisitions of complete maps of all magnetic field vector components for both proton and heteronuclear MR coils of arbitrary geometrical shapes. The advantage of the method proposed here, compared with methods based on measurements with an MR-scanner, is that a complete image of both receive and transmit B<sub>1</sub>-fields, including the phase of the B<sub>1</sub>-field, can be acquired. The B<sub>1</sub> field maps obtained in this manner can be used for absolute quantification of metabolites in MRS experiments, as well as for intensity compensations in imaging experiments, both of which are important concepts in biological and medical MR applications. Another use might be in coil development and testing. A comparison with B<sub>1</sub> field magnitude maps obtained with an MR-scanner was included to validate the accuracy of the proposed method.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 4","pages":"Article 184307"},"PeriodicalIF":3.4,"publicationDate":"2024-02-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139970860","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}
Gustavo Almeida e Silva , Vinícius Galvão Wakui , Lucília Kato , Cássia A. Marquezin
{"title":"Spectroscopic behavior of bufotenine and bufotenine N-oxide: Solvent and pH effects and interaction with biomembrane models","authors":"Gustavo Almeida e Silva , Vinícius Galvão Wakui , Lucília Kato , Cássia A. Marquezin","doi":"10.1016/j.bbamem.2024.184304","DOIUrl":"10.1016/j.bbamem.2024.184304","url":null,"abstract":"<div><p>Bufotenine is a fluorescent analog of Dimethyltryptamine (DMT) that has been widely studied due to its psychedelic properties and biological activity. However, little is known about its spectroscopic properties in different media. Thus, we present in this work, for the first time, the spectroscopic behavior of bufotenine and bufotenine N-oxide by means of their fluorescence properties. Both molecules exhibit changes in optical absorption and emission spectra with variations in pH of the medium and in different solvents. Assays in the presence of biomembranes models, like micelles and liposomes, were also performed. In surfactants titration experiments, the spectral shift observed in fluorescence shows the interaction of both molecules with pre-micellar structures and with micelles. Steady state anisotropy measurements show that both bufotenine and bufotenine N-oxide, in the studied concentration range, interact with liposomes without causing changes in the fluidity of the lipid bilayer. These results can be useful in studies that aim at searching for new compounds, inspired by bufotenine and bufotenine N-oxide, with relevant pharmacological activities and also in studies that use these molecules as markers of psychiatric disorders.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 4","pages":"Article 184304"},"PeriodicalIF":3.4,"publicationDate":"2024-02-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139970862","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":"Structure and mechanism of the human copper transporting ATPases: Fitting the pieces into a moving puzzle","authors":"Oleg Y. Dmitriev, Jaala Patry","doi":"10.1016/j.bbamem.2024.184306","DOIUrl":"10.1016/j.bbamem.2024.184306","url":null,"abstract":"<div><p>Human copper transporters ATP7B and ATP7A deliver copper to biosynthetic pathways and maintain copper homeostasis in the cell. These enzymes combine several challenges for structural biology because they are large low abundance membrane proteins with many highly mobile domains and long disordered loops. No method has yet succeeded in solving the structure of the complete fully functional protein. Still, X-ray crystallography, Cryo-EM and NMR helped to piece together a structure based model of the enzyme activity and regulation by copper. We review the structures of ATP7B and ATP7A with an emphasis on the mechanistic insights into the unique aspects of the transport function and regulation of the human copper ATPases that have emerged from more than twenty years of research.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 4","pages":"Article 184306"},"PeriodicalIF":3.4,"publicationDate":"2024-02-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0005273624000373/pdfft?md5=bab8aadd2e7be7d1baaed62c896469f1&pid=1-s2.0-S0005273624000373-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139947173","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}
Luiz H.S. Andrilli , Heitor G. Sebinelli , Juçara G. Cominal , Maytê Bolean , Larwsk Hayann , José Luís Millán , Ana P. Ramos , Pietro Ciancaglini
{"title":"Differential effects of the lipidic and ionic microenvironment on NPP1's phosphohydrolase and phosphodiesterase activities","authors":"Luiz H.S. Andrilli , Heitor G. Sebinelli , Juçara G. Cominal , Maytê Bolean , Larwsk Hayann , José Luís Millán , Ana P. Ramos , Pietro Ciancaglini","doi":"10.1016/j.bbamem.2024.184292","DOIUrl":"10.1016/j.bbamem.2024.184292","url":null,"abstract":"<div><p>Ecto-nucleotide pyrophosphatase/phosphodiesterase 1 (NPP1) is an enzyme present in matrix vesicles (MV). NPP1 participates on the regulation of bone formation by producing pyrophosphate (PP<sub>i</sub>) from adenosine triphosphate (ATP). Here, we have used liposomes bearing dipalmitoylphosphatidylcholine (DPPC), sphingomyelin (SM), and cholesterol (Chol) harboring NPP1 to mimic the composition of MV <em>lipid rafts</em> to investigate ionic and lipidic influence on NPP1 activity and mineral propagation. Atomic force microscopy (AFM) revealed that DPPC-liposomes had spherical and smooth surface. The presence of SM and Chol elicited rough and smooth surface, respectively. NPP1 insertion produced protrusions in all the liposome surface. Maximum phosphodiesterase activity emerged at 0.082 M ionic strength, whereas maximum phosphomonohydrolase activity arose at low ionic strength. Phosphoserine-Calcium Phosphate Complex (PS-CPLX) and amorphous calcium-phosphate (ACP) induced mineral propagation in DPPC- and DPPC:SM-liposomes and in DPPC:Chol-liposomes, respectively. Mineral characterization revealed the presence of bands assigned to HAp in the mineral propagated by NPP1 harbored in DPPC-liposomes without nucleators or in DPPC:Chol-liposomes with ACP nucleators. These data show that studying how the ionic and lipidic environment affects NPP1 properties is important, especially for HAp obtained under controlled conditions in vitro.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 4","pages":"Article 184292"},"PeriodicalIF":3.4,"publicationDate":"2024-02-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139717340","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}
Anita Wnętrzak , Dawid Szymczuk , Anna Chachaj-Brekiesz , Patrycja Dynarowicz-Latka , Dawid Lupa , Ewelina W. Lipiec , Paulina Laszuk , Aneta D. Petelska , Karolina H. Markiewicz , Agnieszka Z. Wilczewska
{"title":"Lithocholic acid-based oligomers as drug delivery candidates targeting model of lipid raft","authors":"Anita Wnętrzak , Dawid Szymczuk , Anna Chachaj-Brekiesz , Patrycja Dynarowicz-Latka , Dawid Lupa , Ewelina W. Lipiec , Paulina Laszuk , Aneta D. Petelska , Karolina H. Markiewicz , Agnieszka Z. Wilczewska","doi":"10.1016/j.bbamem.2024.184294","DOIUrl":"10.1016/j.bbamem.2024.184294","url":null,"abstract":"<div><p>This study presents a new approach to designing a lithocholic acid functionalized oligomer (OLithocholicAA-X) that can be used as a drug carrier with additional, beneficial activity. Namely, this novel oligomer can incorporate an anti-cancer drug due to the application of an effective backbone as its component (lithocholic acid) alone is known to have anticancer activity. The oligomer was synthesized and characterized in detail by nuclear magnetic resonance, attenuated total reflectance Fourier-transform infrared spectroscopy, ultraviolet-visible spectroscopy, thermal analysis, and mass spectrometry analysis. We selected lipid rafts as potential drug carrier-membrane binding sites. In this respect, we investigated the effects of OLithocholicAA-X on model lipid raft of normal and altered composition, containing an increased amount of cholesterol (Chol) or sphingomyelin (SM), using Langmuir monolayers and liposomes. The surface topography of the studied monolayers was additionally investigated by atomic force microscopy (AFM). The obtained results showed that the investigated oligomer has affinity for a system that mimics a normal lipid raft (SM:Chol 2:1). On the other hand, for systems with an excess of SM or Chol, thermodynamically unfavorable fluidization of the films occurs. Moreover, AFM topographies showed that the amount of SM determines the bioavailability of the oligomer, causing fragmentation of its lattice.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 3","pages":"Article 184294"},"PeriodicalIF":3.4,"publicationDate":"2024-02-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139662080","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}
Sara N. Moya Betancourt, Candelaria I. Cámara, Ana V. Juarez, Julieta S. Riva
{"title":"Magnetically controlled insertion of magnetic nanoparticles into membrane model","authors":"Sara N. Moya Betancourt, Candelaria I. Cámara, Ana V. Juarez, Julieta S. Riva","doi":"10.1016/j.bbamem.2024.184293","DOIUrl":"10.1016/j.bbamem.2024.184293","url":null,"abstract":"<div><p>Polysaccharide–coated magnetic nanoparticles (MNPs) have been reported to show potential applications in many biomedical fields. In this report, we have studied the interactions between magnetite (Fe<sub>3</sub>O<sub>4</sub>) MNPs functionalized with polysaccharides (diethylamino–ethyl dextran, DEAE–D or chitosan, CHI) with different membranes models by Langmuir isotherms, incorporation experiments, and brewster angle microscopy (BAM). In this report, zwitterionic 1,2–distearoyl–sn–glycerol–3–phosphoethanolamine (DSPE) and anionic 1,2–distearoyl–sn–glycerol–3–phosphate (DSPA) phospholipid, were used to form membrane models. Incorporation experiments (π–t) as well as the compression isotherms demonstrate positive interactions between MNPs and DSPE or DSPA monolayers. The study assessed the impact of varying initial surface pressure on a preformed phospholipid monolayer to determine the maximum insertion pressure (MIP) and synergy. Our findings indicate that the primary driving force of the coated MNPs incorporation into the monolayer predominantly stems from electrostatic interaction. The drop in the subphase pH from 6.0 to 4.0 led to an enhancement of the MIP value for DSPA phospholipid monolayer. On the other hand, for DSPE, the drop in the pH does not affect the MIP values. Besides, the presence of a magnetic field induces an enhancement of the insertion process of the MNPs into DSPA preformed monolayer, demonstrating that a previous interaction between MNPs and phospholipid preformed monolayer needs to take place to enhance the incorporation process. This work opens novel perspectives for the research of the influence of magnetic fields on the incorporation of MNPs into model membranes.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 3","pages":"Article 184293"},"PeriodicalIF":3.4,"publicationDate":"2024-02-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139662111","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}
Tancredi Bin , Giovanni Venturoli , Anna Maria Ghelli , Francesco Francia
{"title":"Use of bacterial photosynthetic vesicles to evaluate the effect of ionic liquids on the permeability of biological membranes","authors":"Tancredi Bin , Giovanni Venturoli , Anna Maria Ghelli , Francesco Francia","doi":"10.1016/j.bbamem.2024.184291","DOIUrl":"10.1016/j.bbamem.2024.184291","url":null,"abstract":"<div><p>Ionic liquids (ILs) are salts composed of a combination of organic or inorganic cations and anions characterized by a low melting point, often below 100 °C. This property, together with an extremely low vapor pressure, low flammability and high thermal stability, makes them suitable for replacing canonical organic solvents, with a reduction of industrial activities impact on the environment. Although in the last decades the eco-compatibility of ILs has been extensively verified through toxicological tests performed on model organisms, a detailed understanding of the interaction of these compounds with biological membranes is far from being exhaustive. In this context, we have chosen to evaluate the effect of some ILs on native membranes by using chromatophores, photosynthetic vesicles that can be isolated from <em>Rhodobacter capsulatus</em>, a member of the purple non‑sulfur bacteria. Here, carotenoids associated with the light-harvesting complex II, act as endogenous spectral probes of the transmembrane electrical potential (ΔΨ). By measuring through time-resolved absorption spectroscopy the evolution of the carotenoid band shift induced by a single excitation of the photosynthetic reaction center, information on the ΔΨ dissipation due to ionic currents across the membrane can be obtained. We found that some ILs cause a rather fast dissipation of the transmembrane ΔΨ even at low concentrations, and that this behavior is dose-dependent. By using two different models to analyze the decay of the carotenoid signals, we attempted to interpret at a mechanistic level the marked increase of ionic permeability caused by specific ILs.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 3","pages":"Article 184291"},"PeriodicalIF":3.4,"publicationDate":"2024-01-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139646689","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}
Jessica Múnera-Jaramillo , Gerson-Dirceu López , Elizabeth Suesca , Chiara Carazzone , Chad Leidy , Marcela Manrique-Moreno
{"title":"The role of staphyloxanthin in the regulation of membrane biophysical properties in Staphylococcus aureus","authors":"Jessica Múnera-Jaramillo , Gerson-Dirceu López , Elizabeth Suesca , Chiara Carazzone , Chad Leidy , Marcela Manrique-Moreno","doi":"10.1016/j.bbamem.2024.184288","DOIUrl":"10.1016/j.bbamem.2024.184288","url":null,"abstract":"<div><p><span><em>Staphylococcus aureus</em></span><span><span> is an opportunistic pathogen that is considered a global health threat. This microorganism can adapt to hostile conditions by regulating membrane lipid composition in response to external stress factors such as changes in pH and </span>ionic strength. </span><em>S. aureus</em><span><span> synthesizes and incorporates in its membrane staphyloxanthin, a carotenoid<span><span> providing protection against oxidative damage and antimicrobial agents. Staphyloxanthin is known to modulate the physical properties of the bacterial membranes due to the rigid diaponeurosporenoic group it contains. In this work, preparative </span>thin layer chromatography and </span></span>liquid chromatography mass spectrometry were used to purify staphyloxanthin from </span><em>S. aureus</em> and characterize its structure, identifying C15, C17 and C19 as the main fatty acids in this carotenoid. Changes in the biophysical properties of models of <em>S. aureus</em><span><span> membranes containing phosphatidylglycerol, </span>cardiolipin, and staphyloxanthin were evaluated. Infrared spectroscopy shows that staphyloxanthin reduces the liquid-crystalline to gel phase transition temperature in the evaluated model systems. Interestingly, these shifts are not accompanied by strong changes in </span><em>trans</em>/<em>gauche</em><span><span> isomerization<span>, indicating that chain conformation in the liquid-crystalline phase is not altered by staphyloxanthin. In contrast, headgroup spacing, measured by Laurdan GP fluorescence spectroscopy, and </span></span>lipid<span> core dynamics, measured by DPH fluorescence anisotropy, show significant shifts in the presence of staphyloxanthin. The combined results show that staphyloxanthin reduces lipid core dynamics and headgroup spacing without altering acyl chain conformations, therefore decoupling these normally correlated effects. We propose that the rigid diaponeurosporenoic group in staphyloxanthin and its positioning in the membrane is likely responsible for the results observed.</span></span></p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 3","pages":"Article 184288"},"PeriodicalIF":3.4,"publicationDate":"2024-01-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139575139","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}
I. Orlovska , G. Zubova , O. Shatursky , O. Kukharenko , O. Podolich , T. Gorid'ko , H. Kosyakova , T. Borisova , N. Kozyrovska
{"title":"Extracellular membrane vesicles derived from Komagataeibacter oboediens exposed on the International Space Station fuse with artificial eukaryotic membranes in contrast to vesicles of reference bacterium","authors":"I. Orlovska , G. Zubova , O. Shatursky , O. Kukharenko , O. Podolich , T. Gorid'ko , H. Kosyakova , T. Borisova , N. Kozyrovska","doi":"10.1016/j.bbamem.2024.184290","DOIUrl":"10.1016/j.bbamem.2024.184290","url":null,"abstract":"<div><p>Membranous Extracellular Vesicles (EVs) of Gram-negative bacteria are a secretion and delivery system that can disseminate bacterial products and interact with hosts and the environment. EVs of nonpathogenic bacteria deliver their contents by endocytosis into eukaryotic cells, however, no evidence exists for a fusion delivery mechanism. Here, we describe the fusion of exposed to space/Mars-like stressors simulated on the International Space Station vesicles (<em>E</em>-EVs) from <em>Komagataeibacter oboediens</em> to different types of model planar membranes in comparison with the EVs of the ground-based reference strain. The most reliable fusion was achieved with PC:PE:ergosterol or sterol-free PC:PE bilayers. The relative permeability ratio (PK+/PCl-) estimated from the shift of zero current potential according to Goldman–Hodgkin–Katz equation consisted of 4.17 ± 0.48, which coincides with preferential cation selectivity of the EV endogenous channels. The increase in membrane potential from 50 mV to 100 mV induced the fusion of <em>E</em>-EVs with all tested lipid compositions. The fusion of model exosomes with planar bilayer lipid membranes was confirmed by separate step-like increases in its conductance. In contrast, the ground-based reference <em>K. oboediens</em> EVs never induced the fusion event. In our study, we show membrane lipidome perturbations and increased protein aggregation occurred in the exposed samples in the harsh environment when outer membranes of <em>K. oboediens</em> acquired the capability of both homo- and heterotypic fusion possibly by altered membrane fluidity and the pore-forming capability.</p></div>","PeriodicalId":8831,"journal":{"name":"Biochimica et biophysica acta. Biomembranes","volume":"1866 3","pages":"Article 184290"},"PeriodicalIF":3.4,"publicationDate":"2024-01-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139569863","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}