{"title":"Lipopolysaccharide increases exosomes secretion from endothelial progenitor cells by toll-like receptor 4 dependent mechanism","authors":"Liang Xia, Xiaotian Wang, Weidong Yao, Meihui Wang, Junhui Zhu","doi":"10.1111/boc.202100086","DOIUrl":"10.1111/boc.202100086","url":null,"abstract":"<div>\u0000 \u0000 \u0000 <section>\u0000 \u0000 <h3> Background Information</h3>\u0000 \u0000 <p>Endothelial progenitor cells (EPCs) can exert angiogenic effects by a paracrine mechanism, where exosomes work as an important mediator. Recent studies reported functional expression of toll-like receptor (TLR) 4 on human EPCs and dose-dependent effects of lipopolysaccharide (LPS) on EPC angiogenic properties. To study the effects of TLR4/LPS signaling on EPC-derived exosomes (Exo) and clarify the mechanism, we investigated the role of LPS on exosomes secretion from human EPCs and tested their anti-oxidation/senescence functions. We employed the inhibitors of the plasma membrane Ca<sup>2+</sup>-ATPase (PMCA), endoplasmic reticulum Ca<sup>2+</sup>-ATPase (ERCA), PLC-IP<sub>3</sub> pathway and store-operated calcium entry to assess the effects of LPS on EPC intracellular calcium signalings which critical for exosome secretion.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Results</h3>\u0000 \u0000 <p>LPS induced the release of Exo in a TLR4-dependent manner in vitro, which effect can be partly abrogated by an membrane-permeable IP <sub>3</sub> R antagonist, 2-aminoethyl diphenylborinate (2-APB), but not PLC inhibitor, U-73122. The LPS can significantly delay the fallback of [Ca<sup>2+</sup>]i after isolating the cellular PMCA activity, and disturb PMCA 1/4 expression. The distribution of elevated intracellular calcium seemed coincident with the development of the multivesicular bodies (MVBs). furthermore, the anti-oxidation/senescence properties of LPS-induced Exo were validated by the senescence-associated β-galactosidase activity assay and reactive oxygen species (ROS) related H<sub>2</sub>DCF-DA assay.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Conclusions</h3>\u0000 \u0000 <p>The mechanism of PMCA downregulation and IP<sub>3</sub>R-dependent ER Ca<sup>2+</sup> release may contribute to the pro-exosomal effects of LPS on EPCs.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Significance</h3>\u0000 \u0000 <p>This study provides new insights into the potential role of LPS/TLR4 pathway in regulating EPC-derived exosomes, which may help to develop some feasible approach to manipulate the Exo secretion and promote the clinical application of EPCs therapy in future.</p>\u0000 </section>\u0000 </div>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":null,"pages":null},"PeriodicalIF":2.7,"publicationDate":"2022-03-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"46757185","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Melanie Tingler, Melanie Philipp, Martin D. Burkhalter
{"title":"DNA Replication proteins in primary microcephaly syndromes","authors":"Melanie Tingler, Melanie Philipp, Martin D. Burkhalter","doi":"10.1111/boc.202100061","DOIUrl":"10.1111/boc.202100061","url":null,"abstract":"<p>Improper expansion of neural stem and progenitor cells during brain development manifests in primary microcephaly. This disease is characterized by a reduced head circumference, which correlates with a reduction in brain size. This often corresponds to a general underdevelopment of the brain and entails cognitive, behavioral and motoric retardation. In the past decade significant research efforts have been undertaken to identify genes and the molecular mechanisms underlying microcephaly. One such gene set encompasses factors required for DNA replication. Intriguingly, a growing body of evidence indicates that a substantial number of these genes mediate faithful centrosome and cilium function in addition to their canonical function in genome duplication. Here, we summarize, which DNA replication factors are associated with microcephaly syndromes and to which extent they impact on centrosomes and cilia.</p>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":null,"pages":null},"PeriodicalIF":2.7,"publicationDate":"2022-02-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/boc.202100061","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39633890","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Alexandra Triantafyllou, Maria Gazouli, Charalampos Theodoropoulos, Eleni Zografos, George C. Zografos, Nikolaos V. Michalopoulos
{"title":"Exosomes in breast cancer management: Where do we stand? A literature review","authors":"Alexandra Triantafyllou, Maria Gazouli, Charalampos Theodoropoulos, Eleni Zografos, George C. Zografos, Nikolaos V. Michalopoulos","doi":"10.1111/boc.202100081","DOIUrl":"10.1111/boc.202100081","url":null,"abstract":"<div>\u0000 \u0000 \u0000 <section>\u0000 \u0000 <h3> Background</h3>\u0000 \u0000 <p>Exosomes constitute cellular molecular fingertips that participate in intercellular communication both in health and disease states. Hence, exosomes emerge as critical mediators of cancer development and progression, as well as potential biomarkers and novel therapeutic targets.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Objective</h3>\u0000 \u0000 <p>To review literature data regarding applications of circulating exosomes in breast cancer management.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Methods</h3>\u0000 \u0000 <p>This is a literature review of relevant published studies until April 2020 in PubMed and Google Scholar databases. Original papers in the English language concerning exosome related studies were included.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Results</h3>\u0000 \u0000 <p>Exosomes represent molecular miniatures of their parent cells. Several homeostatic mechanisms control exosomal secretion and synthesis. Exosomal exchange among cells creates an intricate intercellular crosstalk orchestrating almost every tissue process, as well as carcinogenesis. Available data highlight exosomes as major mediators of cancer development and progression. The secretion of specific exosomal molecules, particularly miRNAs, correlates with the underlying processes and can be used as a means of tumor detection and prognostic assessment.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Conclusions</h3>\u0000 \u0000 <p>Exosomal miRNAs expression profiles and levels closely relate to cancer extent, type and prognosis. Deep comprehension of such correlations and systematization of experimental outcomes will offer a novel approach in cancer detection and management.</p>\u0000 </section>\u0000 </div>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":null,"pages":null},"PeriodicalIF":2.7,"publicationDate":"2022-01-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39859729","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Label-free 3D characterization of cardiac fibrosis in muscular dystrophy using SHG imaging of cleared tissue","authors":"Julien Pichon, Mireille Ledevin, Thibaut Larcher, Frédéric Jamme, Karl Rouger, Laurence Dubreil","doi":"10.1111/boc.202100056","DOIUrl":"10.1111/boc.202100056","url":null,"abstract":"<div>\u0000 \u0000 \u0000 <section>\u0000 \u0000 <h3> Background information</h3>\u0000 \u0000 <p>Duchenne muscular dystrophy (DMD) is a neuromuscular disease caused by mutations in the gene encoding dystrophin. It leads to repeated cycles of muscle fiber necrosis and regeneration and progressive replacement of fibers by fibrotic and adipose tissue, with consequent muscle weakness and premature death. Fibrosis and, in particular, collagen accumulation are important pathological features of dystrophic muscle. A better understanding of the development of fibrosis is crucial to enable better management of DMD. Three-dimensional (3D) characterization of collagen organization by second harmonic generation (SHG) microscopy has already proven a highly informative means of studying the fibrotic network in tissue.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Results</h3>\u0000 \u0000 <p>Here, we combine for the first-time tissue clearing with SHG microscopy to characterize in depth the 3D cardiac fibrosis network from DMD<sup>mdx</sup> rat model. Heart sections (1-mm-thick) from 1-year-old wild-type (WT) and DMD<sup>mdx</sup> rats were cleared using the CUBIC protocol. SHG microscopy revealed significantly greater collagen deposition in DMD<sup>mdx</sup> versus WT sections. Analyses revealed a specific pattern of SHG<sup>+</sup> segmented objects in DMD<sup>mdx</sup> cardiac muscle, characterized by a less elongated shape and increased density. Compared with the observed alignment of SHG<sup>+</sup> collagen fibers in WT rats, profound fiber disorganization was observed in DMD<sup>mdx</sup> rats, in which we observed two distinct SHG<sup>+</sup> collagen fiber profiles, which may reflect two distinct stages of the fibrotic process in DMD.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Conclusion and significance</h3>\u0000 \u0000 <p>The current work highlights the interest to combine multiphoton SHG microscopy and tissue clearing for 3D fibrosis network characterization in label free organ. It could be a relevant tool to characterize the fibrotic tissue remodeling in relation to the disease progression and/or to evaluate the efficacy of therapeutic strategies in preclinical studies in DMD model or others fibrosis-related cardiomyopathies diseases.</p>\u0000 </section>\u0000 </div>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":null,"pages":null},"PeriodicalIF":2.7,"publicationDate":"2021-12-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39772240","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Human breast tumor derived endothelial cells exhibit distinct biological properties","authors":"Mangala Hegde, Sharath Mohan Bhat, Kanive Parashiva Guruprasad, Rajasekhar Moka, Lingadakai Ramachandra, Kapaettu Satyamoorthy, Manjunath B. Joshi","doi":"10.1111/boc.202100015","DOIUrl":"10.1111/boc.202100015","url":null,"abstract":"<div>\u0000 \u0000 \u0000 <section>\u0000 \u0000 <h3> Background Information</h3>\u0000 \u0000 <p>Excessive angiogenesis characterized by leaky, tortuous, and chaotic vasculature is one of the hallmarks of cancers and is significantly correlated to poor prognosis. Disorganized angiogenesis leads to poor perfusion of anti-cancer drugs and limits access to immune cells. Hence, impeding angiogenesis is one of the attractive therapeutic targets to inhibit progression and metastasis in several solid tumors including breast.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Results</h3>\u0000 \u0000 <p>We have developed a robust and reproducible method for isolating and ex vivo culture of endothelial cells (EC) derived from non-malignant (Endo-N) and malignant (Endo-T) part from clinically characterized human breast tumors. RT-PCR and immunoblotting analysis indicated that these cells exhibited expression of endothelial specific genes such as PECAM-1 (CD31), Endoglin (CD105), eNOS, VE-cadherin, VCAM1, and MCAM. Vasculogenic mimicry and contamination of progenitor EC recruited in tumors was ruled out by absence of CD133 expression and normal karyotype. Both the cell types showed stable expression of CD31 and CD105 up to seven passages. Furthermore, compared to Endo-N cells, Endo-T cells showed (a) constitutively increased proliferation marked by nearly 36% of cells in mitotic phase, (b) requirement of glutamine for cell survival, (c) pro-migratory phenotype, (d) produced increased number of sprouts in 3D cultures, and (e) resistance to sorafenib.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Conclusion</h3>\u0000 \u0000 <p>Tumor derived EC showed distinct biological properties compared to normal breast EC.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Significance</h3>\u0000 \u0000 <p>Our method for isolating endothelial cell types from human breast tumors may be explored to (a) understand cellular and molecular mechanisms, (b) screen anti-angiogenic molecules, and (c) formulate organoid cultures to develop personalized medicine facilitating better clinical management of breast cancers.</p>\u0000 </section>\u0000 </div>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":null,"pages":null},"PeriodicalIF":2.7,"publicationDate":"2021-11-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39872741","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"How palmitoylation affects trafficking and signaling of membrane receptors","authors":"Maxime Jansen, Bruno Beaumelle","doi":"10.1111/boc.202100052","DOIUrl":"10.1111/boc.202100052","url":null,"abstract":"<p>S-acylation (or palmitoylation) is a reversible post-translational modification (PTM) that modulates protein activity, signalization and trafficking. Palmitoylation was found to significantly impact the activity of various membrane receptors involved in either pathogen entry, such as CCR5 (for HIV) and anthrax toxin receptors, cell proliferation (epidermal growth factor receptor), cardiac function (β-Adrenergic receptor), or synaptic function (AMPA receptor). Palmitoylation of these membrane receptors indeed affects not only their internalization, localization, and activation, but also other PTMs such as phosphorylation. In this review, we discuss recent results showing how palmitoylation differently affects the biology of these membrane receptors.</p>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":null,"pages":null},"PeriodicalIF":2.7,"publicationDate":"2021-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39592692","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Issue Information","authors":"","doi":"10.1111/boc.202170022","DOIUrl":"https://doi.org/10.1111/boc.202170022","url":null,"abstract":"","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":null,"pages":null},"PeriodicalIF":2.7,"publicationDate":"2021-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"46117242","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Biology of the CellPub Date : 2021-11-01Epub Date: 2021-10-14DOI: 10.1111/boc.202100072
Sébastien Léon
{"title":"Endocytosis and stress: From mechanisms to cellular physiology.","authors":"Sébastien Léon","doi":"10.1111/boc.202100072","DOIUrl":"https://doi.org/10.1111/boc.202100072","url":null,"abstract":"This issue presents a series of articles and reviews on the theme “Endocytosis and stress.” The purpose of this issue was to cover various aspects of the functions of endocytosis, but also in a variety of model organisms to highlight how this conserved process has been exploited throughout evolution. A series of reviews highlight connections between endocytosis and the properties of the extracellular environment, including signaling molecules, nutrient availability, or biophysical constraints, as well as the importance of endocytosis in cellular function, adaptation, and pathologies. The plethora of cellular functions regulated by endocytosis is well discussed by Giangreco et al. (2021) who provide a series of examples illustrating the various functions of endocytic proteins in cellular physiology, and the pathologies derived from their malfunction. This includes the role of adaptor proteins in clathrinmediated endocytosis (CME) and non-clathrin-mediated endocytosis (NCE), how this regulates signaling pathways, and the links with tumorigenesis.Two reviews then detail the connections between endocytosis and the regulation of signaling pathways. Wu et al. (2021) focus on the mechanisms by which Wnt signaling, a key pathway in development and morphogenesis in animals, is regulated by endocytosis and endosomal trafficking. They notably highlight work in Caenorhabditis elegans on the involvement in Wnt signaling and stress response. Seib and Klein (2021) then discuss the role of endocytosis in the activation of Notch signaling. They mention the importance of endocytosis in generating pulling forces leading to Notch cleavage, a crucial step in Notch pathway activation, but also additional functions in the recycling of Notch ligands. The interplay between membrane tension and CME is carefully reviewed by Djakbarova et al. (2021). The importance of membrane tension in physiological processes such as cell division, migration, or spreading is also underscored. In their monograph, the authors detail how membrane tension is established, regulated, and how this regulates CME. Two additional reviews focus on the regulation of nutrient transporters by endocytosis. Ivanov and Vert (2021) describe the exquisite molecular mechanisms by which","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":null,"pages":null},"PeriodicalIF":2.7,"publicationDate":"2021-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39516685","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Biology of the CellPub Date : 2021-11-01Epub Date: 2021-08-20DOI: 10.1111/boc.202100014
Surabhi Sonam, Clémence Vigouroux, Antoine Jégou, Guillaume Romet-Lemonne, Christophe Le Clainche, Benoit Ladoux, René Marc Mège
{"title":"Direct measurement of near-nano-Newton forces developed by self-organizing actomyosin fibers bound α-catenin.","authors":"Surabhi Sonam, Clémence Vigouroux, Antoine Jégou, Guillaume Romet-Lemonne, Christophe Le Clainche, Benoit Ladoux, René Marc Mège","doi":"10.1111/boc.202100014","DOIUrl":"https://doi.org/10.1111/boc.202100014","url":null,"abstract":"<p><strong>Background information: </strong>Actin cytoskeleton contractility plays a critical role in morphogenetic processes by generating forces that are then transmitted to cell-cell and cell-ECM adhesion complexes. In turn, mechanical properties of the environment are sensed and transmitted to the cytoskeleton at cell adhesion sites, influencing cellular processes such as cell migration, differentiation and survival. Anchoring of the actomyosin cytoskeleton to adhesion sites is mediated by adaptor proteins such as talin or α-catenin that link F-actin to transmembrane cell adhesion receptors, thereby allowing mechanical coupling between the intracellular and extracellular compartments. Thus, a key issue is to be able to measure the forces generated by actomyosin and transmitted to the adhesion complexes. Approaches developed in cells and those probing single molecule mechanical properties of α-catenin molecules allowed to identify α-catenin, an F-actin binding protein which binds to the cadherin complexes as a major player in cadherin-based mechanotransduction. However, it is still very difficult to bridge intercellular forces measured at cellular levels and those measured at the single-molecule level.</p><p><strong>Results: </strong>Here, we applied an intermediate approach allowing reconstruction of the actomyosin-α-catenin complex in acellular conditions to probe directly the transmitted forces. For this, we combined micropatterning of purified α-catenin and spontaneous actomyosin network assembly in the presence of G-actin and Myosin II with microforce sensor arrays used so far to measure cell-generated forces.</p><p><strong>Conclusions: </strong>Using this method, we show that self-organizing actomyosin bundles bound to micrometric α-catenin patches can apply near-nano-Newton forces.</p><p><strong>Significance: </strong>Our results pave the way for future studies on molecular/cellular mechanotransduction and mechanosensing.</p>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":null,"pages":null},"PeriodicalIF":2.7,"publicationDate":"2021-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39205106","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Bioengineering methods for organoid systems","authors":"Jad Saleh, Barbara Mercier, Wang XI","doi":"10.1111/boc.202000119","DOIUrl":"10.1111/boc.202000119","url":null,"abstract":"<p>Organoids have been widely used in fundamental, biomimetic, and therapeutic studies. These multicellular systems form via cell-autonomous self-organization where a cohort of stem cells undergoes in vivo-like proliferation, differentiation, and morphogenesis. They also recapitulate a series of physiological cell organization, complexity and functions that are untouchable by conventional bio-model systems using immortal cell lines. However, the development of organoids is often not easily controlled and their shape and size are yet fully physiological. Recent research has demonstrated that multiple bioengineering tools could be harnessed to control important internal and external cues that dictate stem cell behavior and stem-cell based organoid development. In this review, we introduce the current development of organoid systems and their potentials, as well as their limitations that impede their further utility in research and clinical fields. In comparison to conventional autonomous organoid system, we then review bioengineering approaches that offer improved control over organoid growth and development. We focus on the genetic editing tools that allow the program of build-in responses and phenotypes for organoid systems with enhanced physiological relevance. We also highlight the advances in bioengineering methods to modify cellular external milieus to generate desirable cell composition, 3D micro-architectures, and complex microfluidic systems. We conclude that the emerging biomimetic methods that employ multidisciplinary approaches could prevail in the future development of organoid systems.</p>","PeriodicalId":8859,"journal":{"name":"Biology of the Cell","volume":null,"pages":null},"PeriodicalIF":2.7,"publicationDate":"2021-09-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39464227","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}