Journal of Biological Chemistry最新文献

{"title":"Biochemical and genomic evidence for converging metabolic routes of metformin and biguanide breakdown in environmental Pseudomonads.","authors":"Katie B Wissbroecker, Anthony J Zmuda, Harsheeth Karumanchi, Thomas D Niehaus","doi":"10.1016/j.jbc.2024.107935","DOIUrl":"https://doi.org/10.1016/j.jbc.2024.107935","url":null,"abstract":"<p><p>Metformin is commonly used to lower blood glucose levels and is one of the most widely used pharmaceuticals worldwide. Typical doses are high (0.5-2.0 g day^-1) and the majority travels through the digestive system unabsorbed and enters the wastewater system. Metformin isn't removed by standard wastewater treatments and eventually enters freshwater systems, where it can form N-chloro-derivatives that are toxic to fish and human cells. Thus, metformin is one of the most prevalent anthropogenic pollutants worldwide and there has been considerable interest in finding ways to remove it. We recently isolated Pseudomonads capable of growing on metformin as the sole nitrogen source. We identified candidate genes involved in metformin breakdown through genomic analyses informed by feeding studies. One candidate, a pair of genes that are located on ∼80kb extra-genomic plasmids, was shown to encode a heteromeric Ni-dependent hydrolase that converts metformin to guanylurea and dimethylamine. Metforminase activity of these gene products is now well established as our results confirm three recently published independent studies. Our isolated Pseudomonads also grow on biguanide, suggesting the existence of an additional breakdown enzyme. Another candidate gene located on the ∼80kb plasmids was shown to encode an aminohydrolase that converts biguanide to guanylurea. Biguanide may arise through successive N-demethylations of metformin or come from other sources. Our results suggest that the recent evolution of metforminase and biguanide hydrolase enzymes allow Pseudomonads to convert either metformin or biguanide to guanylurea, which can be assimilated by existing pathways.</p>","PeriodicalId":15140,"journal":{"name":"Journal of Biological Chemistry","volume":null,"pages":null},"PeriodicalIF":4.0,"publicationDate":"2024-10-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142545652","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Defining unique structural features in the MAFA and MAFB transcription factors that control Insulin gene activity.","authors":"Jeeyeon Cha, Xin Tong, Katie C Coate, Min Guo, Jin-Hua Liu, Garrett Reynolds, Emily M Walker, Richard A Stein, Hassane Mchaourab, Roland Stein","doi":"10.1016/j.jbc.2024.107938","DOIUrl":"10.1016/j.jbc.2024.107938","url":null,"abstract":"<p><p>MAFA and MAFB are related basic-leucine-zipper domain-containing transcription factors which have important overlapping and distinct regulatory roles in a variety of cellular contexts, including hormone production in pancreatic islet cells. Here we first examined how mutating conserved MAF protein-DNA contact sites obtained from X-ray crystal structure analysis impacted their DNA-binding and Insulin enhancer-driven activity. While most of these interactions were essential and their disruption severely compromised activity, we identified that regions outside of these contact sites also contributed to transcriptional activity. AlphaFold 2, an artificial intelligence-based structural prediction program, was used to determine if there were also differences in the three-dimensional organization of the non-DNA binding/dimerization sequences of MAFA and MAFB. This analysis was conducted on the wildtype (WT) proteins as well as the pathogenic MAFA^Ser64Phe and MAFB^Ser70Alatrans-activation domain mutants, with differences revealed between MAFA^WT and MAFB^WT as well as between MAFA^Ser64Phe and MAFA^WT, but not between MAFB^Ser70Ala and MAFB^WT. Moreover, dissimilarities between these proteins were also observed in their ability to cooperatively stimulate Insulin enhancer-driven activity in the presence of other islet-enriched transcription factors. Analysis of MAFA and MAFB chimeras disclosed that these properties were influenced by their unique C-terminal region structural differences predicted by AlphaFold 2. Our findings have revealed key structural features of these closely related proteins that impact their ability to regulate gene expression.</p>","PeriodicalId":15140,"journal":{"name":"Journal of Biological Chemistry","volume":null,"pages":null},"PeriodicalIF":4.0,"publicationDate":"2024-10-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142545653","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Functional roles of the [2Fe-2S] clusters in Synechocystis PCC 6803 Hox [NiFe]-hydrogenase reactivity with ferredoxins.","authors":"Matthew R Blahut, Michael E Dawson, Effie C Kisgeropoulos, Anastasia E Ledinina, David W Mulder, Paul W King","doi":"10.1016/j.jbc.2024.107936","DOIUrl":"https://doi.org/10.1016/j.jbc.2024.107936","url":null,"abstract":"<p><p>The HoxEFUYH complex of Synechocystis PCC 6803 (S. 6803) consists of a HoxEFU ferredoxin:NAD(P)H oxidoreductase subcomplex and a HoxYH [NiFe]-hydrogenase subcomplex that catalyzes reversible H₂ oxidation. Prior studies have suggested that the presence of HoxE is required for reactivity with ferredoxin, however, it is unknown how HoxE is functionally integrated into the electron transfer network of the HoxEFU:ferredoxin complex. Deciphering electron transfer pathways is challenged by the rich iron-sulfur cluster content of HoxEFU, which includes a [2Fe-2S] cluster in each subunit, along with multiple [4Fe-4S] clusters and a flavin cofactor. To resolve the role of HoxE, we determined the biophysical and thermodynamic properties of each [2Fe-2S] cluster in HoxEFU using steady-state and potentiometric EPR analysis in combination with square wave voltammetry (SWV). The temperature-dependence of the EPR signal for HoxE confirmed the coordination of a single [2Fe-2S] cluster that was shown by SWV to have an E_m = -424 mV (vs SHE). Strikingly, when the E_m of the HoxE [2Fe-2S] cluster was analyzed in HoxEFU titrations, it was shifted by > 100 mV to an E_m < -525 mV (vs SHE). EPR titrations of HoxEFU gave an E_m value for the [2Fe-2S] cluster of HoxF, E_m = -419 mV and HoxU, E_m = -349 mV. These values were used to re-analyze the diaphorase kinetics in reactions performed with ferredoxins with varying E_m's. The results are formulated into a model of HoxEFU:ferredoxin reactivity and the role of HoxE in mediating electron transfer within the HoxEFU:ferredoxin complex.</p>","PeriodicalId":15140,"journal":{"name":"Journal of Biological Chemistry","volume":null,"pages":null},"PeriodicalIF":4.0,"publicationDate":"2024-10-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142545655","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Transcriptomic and metabolic signatures of neural cells cultured under a physiological-like environment.","authors":"Emilio Fernandez, Moussa Warde, Israel Manjarres-Raza, Veronica Bobo-Jimenez, Maria Martinez-Luna, Carlos Vicente-Gutierrez, Dario Garcia-Rodriguez, Daniel Jimenez-Blasco, Angeles Almeida, Juan P Bolaños","doi":"10.1016/j.jbc.2024.107937","DOIUrl":"https://doi.org/10.1016/j.jbc.2024.107937","url":null,"abstract":"<p><p>Cultured brain cells are used conventionally to investigate fundamental neurobiology and identify therapeutic targets against neural diseases. However, standard culture conditions do not simulate the natural cell microenvironment, thus hampering in vivo translational insight. Major weaknesses include atmospheric (21%) O₂ tension and lack of intercellular communication, two factors likely impacting metabolism and signaling. Here, we addressed this issue in mouse neurons and astrocytes in primary culture. We found that the signs of cellular and mitochondrial integrity were optimal when these cells were acclimated to grow in co-culture, to emulate intercellular coupling, under physiological (5%) O₂ tension. Transcriptomic scrutiny, performed to elucidate the adaptive mechanism involved, revealed that the vast majority of differentially expressed transcripts were downregulated in both astrocytes and neurons. Gene ontology evaluation unveiled that the largest group of altered transcripts was glycolysis, which was experimentally validated by metabolic flux analyses. This protocol and database resource for neural cells grown under in vivo-like microenvironment may move forward the translation of basic into applied neurobiological research.</p>","PeriodicalId":15140,"journal":{"name":"Journal of Biological Chemistry","volume":null,"pages":null},"PeriodicalIF":4.0,"publicationDate":"2024-10-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142545660","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"A peptide derived from the amino terminus of leptin improves glucose metabolism and energy homeostasis in myotubes and db/db mice.","authors":"Mehmood Ali, Arvind Gupta, Rahul Dev Verma, Sariyah Akhtar, Jimut Kanti Ghosh","doi":"10.1016/j.jbc.2024.107919","DOIUrl":"https://doi.org/10.1016/j.jbc.2024.107919","url":null,"abstract":"<p><p>Leptin is an adipokine, which plays key roles in regulation of glucose-metabolism and energy-homeostasis. Therefore, identification of a short peptide from Leptin which improves glucose-metabolism and energy-homeostasis could be of significant therapeutic importance. Mutational studies demonstrated that N-terminal of human Leptin-hormone (LH) is crucial for activation of Leptin-receptor while its C-terminal seems to have lesser effects in it. Thus, for finding a metabolically active peptide and complimenting the mutational studies on Leptin, we have identified a 17-mer (Leptin-1) and a 16-mer (Leptin-2) segment from its N-terminal and C-terminal respectively. Consistent with the mutational studies, Leptin-1 improved glucose-metabolism by increasing glucose-uptake, GLUT4 expression and its translocation to the plasma-membrane in L6-myotubes, while Leptin-2 was mostly inactive. Leptin-1-induced glucose-uptake is mediated through activation of AMPK, PI3K and AKT proteins since inhibitors of these proteins inhibited the event. Leptin-1 activated leptin-receptor immediate downstream target protein, JAK2 reflecting its possible interaction with leptin-receptor while Leptin-2 was less active. Furthermore, Leptin-1 increased mitochondrial-biogenesis and ATP-production, and increased expression of PGC1α, NRF1 and Tfam proteins, that are important regulators of mitochondrial-biogenesis. The results suggested that Leptin-1 improved energy-homeostasis in L6-myotubes, whereas, Leptin-2 showed much lesser effects. In diabetic, db/db mice, Leptin-1 significantly decreased blood glucose level and improved glucose-tolerance. Leptin-1 also increased serum adiponectin and decreased serum TNF-α and IL-6 level signifying the improvement in insulin-sensitivity and decrease in insulin-resistance, respectively in db/db mice. Overall, the results show the identification of a short peptide from the N-terminal of human LH which significantly improves glucose-metabolism and energy-homeostasis.</p>","PeriodicalId":15140,"journal":{"name":"Journal of Biological Chemistry","volume":null,"pages":null},"PeriodicalIF":4.0,"publicationDate":"2024-10-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142568403","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Characterization of atypical BAR domain-containing proteins coded by Toxoplasma gondii.","authors":"Noha Al-Qatabi, Maud Magdeleine, Sophie Pagnotta, Amélie Leforestier, Jéril Degrouard, Ana Andreea Arteni, Sandra Lacas-Gervais, Romain Gautier, Guillaume Drin","doi":"10.1016/j.jbc.2024.107923","DOIUrl":"https://doi.org/10.1016/j.jbc.2024.107923","url":null,"abstract":"<p><p>Toxoplasma gondii, the causative agent of toxoplasmosis, infects cells and replicates inside via the secretion of factors stored in specialized organelles (rhoptries, micronemes, dense granules) and the capture of host materials. The genesis of the secretory organelles and the processes of secretion and endocytosis depend on vesicular trafficking events whose molecular bases remain poorly known. Notably, there is no characterization of the BAR (Bin/Amphiphysin/Rvs) domain-containing proteins expressed by T. gondii and other apicomplexans, although such proteins are known to play critical roles in vesicular trafficking in other eukaryotes. Here, by combining structural analyses with in vitro assays and cellular observations, we have characterized TgREMIND (REgulators of Membrane Interacting Domains), involved in the genesis of rhoptries and dense granules, and TgBAR2 found at the parasite cortex. We establish that TgREMIND comprises an F-BAR domain that can bind curved neutral membranes with no strict phosphoinositide requirement and exert a membrane remodeling activity. Next, we establish that TgREMIND contains a new structural domain called REMIND, which negatively regulates the membrane-binding capacities of the F-BAR domain. In parallel, we report that TgBAR2 contains a BAR domain with an extremely basic membrane-binding interface able to deform anionic membranes into very narrow tubules. Our data show that T. gondii codes for two atypical BAR domain-containing proteins with very contrasting membrane-binding properties, allowing them to function in two distinct regions of the parasite trafficking system.</p>","PeriodicalId":15140,"journal":{"name":"Journal of Biological Chemistry","volume":null,"pages":null},"PeriodicalIF":4.0,"publicationDate":"2024-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142500918","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Crystal structures of cables formed by the acetylated and unacetylated forms of the Schizosaccharomyces pombe tropomyosin orthologue Tpm^Cdc8.","authors":"Patrick Y A Reinke, Robin S Heiringhoff, Theresia Reindl, Karen Baker, Manuel H Taft, Alke Meents, Daniel P Mulvihill, Owen R Davies, Roman Fedorov, Michael Zahn, Dietmar J Manstein","doi":"10.1016/j.jbc.2024.107925","DOIUrl":"https://doi.org/10.1016/j.jbc.2024.107925","url":null,"abstract":"<p><p>Cables formed by head-to-tail polymerization of tropomyosin, localized along the length of sarcomeric and cytoskeletal actin filaments, play a key role in regulating a wide range of motile and contractile processes. The stability of tropomyosin cables, their interaction with actin filaments and the functional properties of the resulting co-filaments are thought to be affected by N-terminal acetylation of tropomyosin. Here, we present high-resolution structures of cables formed by acetylated and unacetylated Schizosaccharomyces pombe tropomyosin orthologue Tpm^Cdc8. The crystal structures represent different types of cables, each consisting of Tpm^Cdc8 homodimers in a different conformation. The structures show how the interactions of the residues in the overlap junction contribute to cable formation and how local structural perturbations affect the conformational dynamics of the protein and its ability to transmit allosteric signals. In particular, N-terminal acetylation increases the helicity of the adjacent region, which leads to a local reduction in conformational dynamics and consequently to less fraying of the N-terminal region. This creates a more consistent complementary surface facilitating the formation of specific interactions across the overlap junction.</p>","PeriodicalId":15140,"journal":{"name":"Journal of Biological Chemistry","volume":null,"pages":null},"PeriodicalIF":4.0,"publicationDate":"2024-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142500919","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Distinct chemical structures inhibit the CEMIP hyaluronidase and promote oligodendrocyte progenitor cell maturation.","authors":"Alec Peters, Fatima Banine, Kanon Yasuhara, Angela Hoffman, Basappa, Prashant K Metri, Lily Gunning, Ava Huffman, Jake VanCampen, Clinton C Shock, Stephen A Back, Larry S Sherman","doi":"10.1016/j.jbc.2024.107916","DOIUrl":"https://doi.org/10.1016/j.jbc.2024.107916","url":null,"abstract":"<p><p>Growing evidence supports pathogenic roles for chronically elevated hyaluronidase activity in numerous conditions. Elevated expression of one such hyaluronidase, the Cell Migration Inducing and hyaluronan binding Protein (CEMIP), has been implicated in the pathogenesis and progression of several cancers as well as demyelinating diseases in the central nervous system (CNS). Developing effective and selective CEMIP inhibitors could therefore have efficacy in treating a variety of conditions where CEMIP is chronically elevated. Using two distinct screens for novel hyaluronidase inhibitors, we identified two synthetic thiocarbamates and one plant-derived flavonoid, sulfuretin, that effectively blocked CEMIP activity in live cells, including a tumorigenic cell line and primary cultures of oligodendrocyte progenitor cells (OPCs). None of these agents influenced cell proliferation, but they had differential dose-dependent and cell type specific effects on cell survival. Furthermore, we found that each of these agents could promote oligodendrocyte maturation by OPCs in the presence of high molecular weight (>2 Mda) hyaluronan, the accumulation of which is linked to the inhibition of OPC maturation and remyelination failure in demyelinating diseases. These findings indicate that CEMIP can be inhibited through distinct chemical interactions, and that CEMIP inhibitors have potential efficacy for treating demyelinating diseases or other conditions where CEMIP is elevated.</p>","PeriodicalId":15140,"journal":{"name":"Journal of Biological Chemistry","volume":null,"pages":null},"PeriodicalIF":4.0,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142500920","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"The activity of the ribonucleotide monophosphatase UmpH is controlled by interaction with the GlnK signaling protein in Escherichia coli.","authors":"Ana Carolina Aparecida Gonçalves, Tatiana de Mello Damasco Nunes, Erick Parize, Edileusa Cristina Marques Gerhardt, Gustavo Antônio de Souza, Jörg Scholl, Karl Forchhammer, Luciano Fernandes Huergo","doi":"10.1016/j.jbc.2024.107931","DOIUrl":"https://doi.org/10.1016/j.jbc.2024.107931","url":null,"abstract":"<p><p>The PII signaling proteins are ubiquitous in prokaryotes serving as crucial metabolic hubs in different metabolic pathways due to their ability to sense and integrate signals of the cellular nitrogen, carbon, and energy levels. In this study we used ligand fishing assays to identify the ribonucleotide monophosphatase UmpH enzyme as a novel target of the PII signaling protein GlnK in Escherichia coli. In vitro analyses showed that UmpH interacts specifically with the PII protein GlnK but not with its paralogue protein GlnB. The UmpH - GlnK complex is modulated by the GlnK uridylylation status and by the levels of the GlnK allosteric effectors ATP, ADP and 2-oxoglutarate. Upon engaging interaction with GlnK, UmpH becomes less active towards its substrate uridine 5'-monophosphate (UMP). We suggest a model where GlnK will physically interact to reduce the UmpH activity during the transition from N-starvation to N-sufficient conditions. Such a mechanism may help the cells to reprogram the fate of UMP from catabolism to anabolism avoiding futile cycling of key nutrients.</p>","PeriodicalId":15140,"journal":{"name":"Journal of Biological Chemistry","volume":null,"pages":null},"PeriodicalIF":4.0,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142500958","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"TFEB agonist clomiphene citrate activates the autophagy-lysosomal pathway and ameliorates Alzheimer's disease symptoms in mice.","authors":"Jieru Lin, Yi Yuan, Chunhuan Huang, Jiayu Zi, Lu Li, Jiamiao Liu, Xiaoting Wu, Wei Li, Qing Zhao, Yuyin Li, Zhenxing Liu, Aipo Diao","doi":"10.1016/j.jbc.2024.107929","DOIUrl":"https://doi.org/10.1016/j.jbc.2024.107929","url":null,"abstract":"<p><p>Autophagy is a conserved eukaryotic cellular clearance and recycling process through the lysosome-mediated degradation of damaged organelles and protein aggregates to maintain homeostasis. Impairment of the autophagy-lysosomal pathway is implicated in the pathogenesis of Alzheimer's disease (AD). Transcription factor EB (TFEB) is a master regulator of autophagy and lysosomal biogenesis. Therefore, activating TFEB and autophagy provides a novel strategy for AD treatment. We previously described that clomiphene citrate (CC) promotes nuclear translocation of TFEB and increases autophagy and lysosomal biogenesis. In this study, 7 and 3-month-old APP/PS1 mice were treated with TFEB agonist CC and assessed. The behavioral tests were performed using Morris water maze and open field test. Additional changes in Aβ pathology, autophagy and inflammatory response were determined. We found that CC activated TFEB and the autophagy-lysosomal pathway in neuronal cells. Moreover, using mouse model of Alzheimer's disease, CC treatment promoted clearance of Aβ plaques and ameliorated cognitive function in both 7 and 3-month-old APP/PS1 mice. The CC-induced activation of TFEB occurs by promoting acetylation of TFEB for nuclear translocation. These findings provide a molecular mechanism for the TFEB-mediated activation of the autophagy-lysosome pathway by CC, which has the potential to be repurposed and applied in the treatment or prevention of AD.</p>","PeriodicalId":15140,"journal":{"name":"Journal of Biological Chemistry","volume":null,"pages":null},"PeriodicalIF":4.0,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142500957","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}