Pub Date : 2024-11-04DOI: 10.1016/j.tcb.2024.10.001
Ivan Milenkovic, Eva Maria Novoa
Ribosomal RNAs (rRNA) are the most abundant RNA molecules in almost all cell types. The general consensus in the field is that rRNA modifications are largely species-specific, with most previous works and databases solely stratifying modifications by the species of origin, without taking other levels of complexity into account. However, new evidence has emerged suggesting dynamic rRNA modifications may have additional layers of complexity and might play an important role in development and disease. In this review article, we summarize recent evidence supporting heterogeneity and dynamics in rRNA modifications in diverse biological contexts, challenging the simplistic view of 'one-species-one-rRNA-modification-pattern'. Moreover, we highlight how rRNA modification dynamics have been studied to date and how long-read sequencing methods can significantly improve our understanding of this largely unexplored yet highly abundant RNA family, across tissues, developmental stages, and diseases.
{"title":"Dynamic rRNA modifications as a source of ribosome heterogeneity.","authors":"Ivan Milenkovic, Eva Maria Novoa","doi":"10.1016/j.tcb.2024.10.001","DOIUrl":"https://doi.org/10.1016/j.tcb.2024.10.001","url":null,"abstract":"<p><p>Ribosomal RNAs (rRNA) are the most abundant RNA molecules in almost all cell types. The general consensus in the field is that rRNA modifications are largely species-specific, with most previous works and databases solely stratifying modifications by the species of origin, without taking other levels of complexity into account. However, new evidence has emerged suggesting dynamic rRNA modifications may have additional layers of complexity and might play an important role in development and disease. In this review article, we summarize recent evidence supporting heterogeneity and dynamics in rRNA modifications in diverse biological contexts, challenging the simplistic view of 'one-species-one-rRNA-modification-pattern'. Moreover, we highlight how rRNA modification dynamics have been studied to date and how long-read sequencing methods can significantly improve our understanding of this largely unexplored yet highly abundant RNA family, across tissues, developmental stages, and diseases.</p>","PeriodicalId":56085,"journal":{"name":"Trends in Cell Biology","volume":null,"pages":null},"PeriodicalIF":13.0,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142585245","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-01Epub Date: 2024-05-21DOI: 10.1016/j.tcb.2024.03.007
Hope E Merens, Karine Choquet, Autum R Baxter-Koenigs, L Stirling Churchman
Splicing is a highly regulated process critical for proper pre-mRNA maturation and the maintenance of a healthy cellular environment. Splicing events are impacted by ongoing transcription, neighboring splicing events, and cis and trans regulatory factors on the respective pre-mRNA transcript. Within this complex regulatory environment, splicing kinetics have the potential to influence splicing outcomes but have historically been challenging to study in vivo. In this review, we highlight recent technological advancements that have enabled measurements of global splicing kinetics and of the variability of splicing kinetics at single introns. We demonstrate how identifying features that are correlated with splicing kinetics has increased our ability to form potential models for how splicing kinetics may be regulated in vivo.
{"title":"Timing is everything: advances in quantifying splicing kinetics.","authors":"Hope E Merens, Karine Choquet, Autum R Baxter-Koenigs, L Stirling Churchman","doi":"10.1016/j.tcb.2024.03.007","DOIUrl":"10.1016/j.tcb.2024.03.007","url":null,"abstract":"<p><p>Splicing is a highly regulated process critical for proper pre-mRNA maturation and the maintenance of a healthy cellular environment. Splicing events are impacted by ongoing transcription, neighboring splicing events, and cis and trans regulatory factors on the respective pre-mRNA transcript. Within this complex regulatory environment, splicing kinetics have the potential to influence splicing outcomes but have historically been challenging to study in vivo. In this review, we highlight recent technological advancements that have enabled measurements of global splicing kinetics and of the variability of splicing kinetics at single introns. We demonstrate how identifying features that are correlated with splicing kinetics has increased our ability to form potential models for how splicing kinetics may be regulated in vivo.</p>","PeriodicalId":56085,"journal":{"name":"Trends in Cell Biology","volume":null,"pages":null},"PeriodicalIF":13.0,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141081871","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-01Epub Date: 2024-10-07DOI: 10.1016/j.tcb.2024.09.002
Chenghao Yan, Xu Liu, Haodong Xu, Liming Wang
Upon various stresses, mtDNA leaks from mitochondria into the cytoplasm, leading to cellular dysfunction and inflammation, thereby exacerbating disease progression. The autophagy-lysosome pathway has emerged as a pivotal quality control mechanism for eliminating abnormal cytoplasmic mtDNA. This article summarizes the mechanisms underlying mtDNA-triggered inflammation and how cytoplasmic mtDNA is eliminated.
{"title":"Cytoplasmic mtDNA clearance suppresses inflammatory immune responses.","authors":"Chenghao Yan, Xu Liu, Haodong Xu, Liming Wang","doi":"10.1016/j.tcb.2024.09.002","DOIUrl":"10.1016/j.tcb.2024.09.002","url":null,"abstract":"<p><p>Upon various stresses, mtDNA leaks from mitochondria into the cytoplasm, leading to cellular dysfunction and inflammation, thereby exacerbating disease progression. The autophagy-lysosome pathway has emerged as a pivotal quality control mechanism for eliminating abnormal cytoplasmic mtDNA. This article summarizes the mechanisms underlying mtDNA-triggered inflammation and how cytoplasmic mtDNA is eliminated.</p>","PeriodicalId":56085,"journal":{"name":"Trends in Cell Biology","volume":null,"pages":null},"PeriodicalIF":13.0,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142395611","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-01Epub Date: 2024-02-10DOI: 10.1016/j.tcb.2024.01.004
Julian Schwärzler, Lisa Mayr, Felix Grabherr, Herbert Tilg, Timon E Adolph
The gut epithelium protects the host from a potentially hostile environment while allowing nutrient uptake that is vital for the organism. To maintain this delicate task, the gut epithelium has evolved multilayered cellular functions ranging from mucus production to hormone release and orchestration of mucosal immunity. Here, we review the execution of intestinal epithelial metabolism in health and illustrate how perturbation of epithelial metabolism affects experimental gut inflammation and tumorigenesis. We also discuss the impact of environmental factors and host-microbe interactions on epithelial metabolism in the context of inflammatory bowel disease and colorectal cancer. Insights into epithelial metabolism hold promise to unravel mechanisms of organismal health that may be therapeutically exploited in humans in the future.
{"title":"Epithelial metabolism as a rheostat for intestinal inflammation and malignancy.","authors":"Julian Schwärzler, Lisa Mayr, Felix Grabherr, Herbert Tilg, Timon E Adolph","doi":"10.1016/j.tcb.2024.01.004","DOIUrl":"10.1016/j.tcb.2024.01.004","url":null,"abstract":"<p><p>The gut epithelium protects the host from a potentially hostile environment while allowing nutrient uptake that is vital for the organism. To maintain this delicate task, the gut epithelium has evolved multilayered cellular functions ranging from mucus production to hormone release and orchestration of mucosal immunity. Here, we review the execution of intestinal epithelial metabolism in health and illustrate how perturbation of epithelial metabolism affects experimental gut inflammation and tumorigenesis. We also discuss the impact of environmental factors and host-microbe interactions on epithelial metabolism in the context of inflammatory bowel disease and colorectal cancer. Insights into epithelial metabolism hold promise to unravel mechanisms of organismal health that may be therapeutically exploited in humans in the future.</p>","PeriodicalId":56085,"journal":{"name":"Trends in Cell Biology","volume":null,"pages":null},"PeriodicalIF":13.0,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139716632","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-01Epub Date: 2024-02-23DOI: 10.1016/j.tcb.2024.01.011
Wonyul Jang, Volker Haucke
Unlike most other organelles found in multiple copies, the endoplasmic reticulum (ER) is a unique singular organelle within eukaryotic cells. Despite its continuous membrane structure, encompassing more than half of the cellular endomembrane system, the ER is subdivided into specialized sub-compartments, including morphological, membrane contact site (MCS), and de novo organelle biogenesis domains. In this review, we discuss recent emerging evidence indicating that, in response to nutrient stress, cells undergo a reorganization of these sub-compartmental ER domains through two main mechanisms: non-destructive remodeling of morphological ER domains via regulation of MCS and organelle hitchhiking, and destructive remodeling of specialized domains by ER-phagy. We further highlight and propose a critical role of membrane lipid metabolism in this ER remodeling during starvation.
{"title":"ER remodeling via lipid metabolism.","authors":"Wonyul Jang, Volker Haucke","doi":"10.1016/j.tcb.2024.01.011","DOIUrl":"10.1016/j.tcb.2024.01.011","url":null,"abstract":"<p><p>Unlike most other organelles found in multiple copies, the endoplasmic reticulum (ER) is a unique singular organelle within eukaryotic cells. Despite its continuous membrane structure, encompassing more than half of the cellular endomembrane system, the ER is subdivided into specialized sub-compartments, including morphological, membrane contact site (MCS), and de novo organelle biogenesis domains. In this review, we discuss recent emerging evidence indicating that, in response to nutrient stress, cells undergo a reorganization of these sub-compartmental ER domains through two main mechanisms: non-destructive remodeling of morphological ER domains via regulation of MCS and organelle hitchhiking, and destructive remodeling of specialized domains by ER-phagy. We further highlight and propose a critical role of membrane lipid metabolism in this ER remodeling during starvation.</p>","PeriodicalId":56085,"journal":{"name":"Trends in Cell Biology","volume":null,"pages":null},"PeriodicalIF":13.0,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139941262","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-01Epub Date: 2023-11-28DOI: 10.1016/j.tcb.2023.10.010
Binghao Chai, Christoforos Efstathiou, Haoran Yue, Viji M Draviam
The growth of artificial intelligence (AI) has led to an increase in the adoption of computer vision and deep learning (DL) techniques for the evaluation of microscopy images and movies. This adoption has not only addressed hurdles in quantitative analysis of dynamic cell biological processes but has also started to support advances in drug development, precision medicine, and genome-phenome mapping. We survey existing AI-based techniques and tools, as well as open-source datasets, with a specific focus on the computational tasks of segmentation, classification, and tracking of cellular and subcellular structures and dynamics. We summarise long-standing challenges in microscopy video analysis from a computational perspective and review emerging research frontiers and innovative applications for DL-guided automation in cell dynamics research.
{"title":"Opportunities and challenges for deep learning in cell dynamics research.","authors":"Binghao Chai, Christoforos Efstathiou, Haoran Yue, Viji M Draviam","doi":"10.1016/j.tcb.2023.10.010","DOIUrl":"10.1016/j.tcb.2023.10.010","url":null,"abstract":"<p><p>The growth of artificial intelligence (AI) has led to an increase in the adoption of computer vision and deep learning (DL) techniques for the evaluation of microscopy images and movies. This adoption has not only addressed hurdles in quantitative analysis of dynamic cell biological processes but has also started to support advances in drug development, precision medicine, and genome-phenome mapping. We survey existing AI-based techniques and tools, as well as open-source datasets, with a specific focus on the computational tasks of segmentation, classification, and tracking of cellular and subcellular structures and dynamics. We summarise long-standing challenges in microscopy video analysis from a computational perspective and review emerging research frontiers and innovative applications for DL-guided automation in cell dynamics research.</p>","PeriodicalId":56085,"journal":{"name":"Trends in Cell Biology","volume":null,"pages":null},"PeriodicalIF":13.0,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138464665","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-01Epub Date: 2024-02-06DOI: 10.1016/j.tcb.2024.01.002
Laura A Claessens, Alfred C O Vertegaal
Posttranslational modification by small ubiquitin-like modifiers (SUMOs) is critical in regulating diverse cellular processes including gene expression, cell cycle progression, genome integrity, cellular metabolism, and inflammation and immunity. The covalent attachment of SUMOs to target proteins is highly dynamic and reversible through the concerted action of SUMO conjugating and deconjugating enzymes. In mammalian cells, sentrin-specific proteases (SENPs) are the most abundant family of deconjugating enzymes. This review highlights recent advances in our knowledge of the substrates and cellular and physiological processes controlled by SENPs. Notably, SENPs are emerging as significant players in cancer, as well as in other diseases, making them attractive targets for therapeutic intervention. Consequently, a growing amount of effort in the field is being directed towards the development of SENP inhibitors.
{"title":"SUMO proteases: from cellular functions to disease.","authors":"Laura A Claessens, Alfred C O Vertegaal","doi":"10.1016/j.tcb.2024.01.002","DOIUrl":"10.1016/j.tcb.2024.01.002","url":null,"abstract":"<p><p>Posttranslational modification by small ubiquitin-like modifiers (SUMOs) is critical in regulating diverse cellular processes including gene expression, cell cycle progression, genome integrity, cellular metabolism, and inflammation and immunity. The covalent attachment of SUMOs to target proteins is highly dynamic and reversible through the concerted action of SUMO conjugating and deconjugating enzymes. In mammalian cells, sentrin-specific proteases (SENPs) are the most abundant family of deconjugating enzymes. This review highlights recent advances in our knowledge of the substrates and cellular and physiological processes controlled by SENPs. Notably, SENPs are emerging as significant players in cancer, as well as in other diseases, making them attractive targets for therapeutic intervention. Consequently, a growing amount of effort in the field is being directed towards the development of SENP inhibitors.</p>","PeriodicalId":56085,"journal":{"name":"Trends in Cell Biology","volume":null,"pages":null},"PeriodicalIF":13.0,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139704140","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-26DOI: 10.1016/j.tcb.2024.09.006
Venkatesh Varadharaj, Wyatt Petersen, Surinder K Batra, Moorthy P Ponnusamy
Glycosylation is a complex co-translational and post-translational modification (PTM) in eukaryotes that utilizes glycosyltransferases to generate a vast array of glycoconjugate structures. Recent studies have highlighted the role of glycans in regulating essential molecular, cellular, tissue, organ, and systemic biological processes with significant implications for human diseases, particularly cancer. The metabolic reliance of cancer, spanning tumor initiation, disease progression, and resistance to therapy, necessitates a range of uniquely altered cellular metabolic pathways. In addition, the intricate interplay between cell-intrinsic and -extrinsic mechanisms is exemplified by the communication between cancer cells, cancer stem cells (CSCs), cancer-associated fibroblasts (CAFs), and immune cells within the tumor microenvironment (TME). In this review article, we explore how differential glycosylation in cancer influences the metabolism and stemness features alongside new avenues in glycobiology.
{"title":"Sugar symphony: glycosylation in cancer metabolism and stemness.","authors":"Venkatesh Varadharaj, Wyatt Petersen, Surinder K Batra, Moorthy P Ponnusamy","doi":"10.1016/j.tcb.2024.09.006","DOIUrl":"https://doi.org/10.1016/j.tcb.2024.09.006","url":null,"abstract":"<p><p>Glycosylation is a complex co-translational and post-translational modification (PTM) in eukaryotes that utilizes glycosyltransferases to generate a vast array of glycoconjugate structures. Recent studies have highlighted the role of glycans in regulating essential molecular, cellular, tissue, organ, and systemic biological processes with significant implications for human diseases, particularly cancer. The metabolic reliance of cancer, spanning tumor initiation, disease progression, and resistance to therapy, necessitates a range of uniquely altered cellular metabolic pathways. In addition, the intricate interplay between cell-intrinsic and -extrinsic mechanisms is exemplified by the communication between cancer cells, cancer stem cells (CSCs), cancer-associated fibroblasts (CAFs), and immune cells within the tumor microenvironment (TME). In this review article, we explore how differential glycosylation in cancer influences the metabolism and stemness features alongside new avenues in glycobiology.</p>","PeriodicalId":56085,"journal":{"name":"Trends in Cell Biology","volume":null,"pages":null},"PeriodicalIF":13.0,"publicationDate":"2024-10-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142513571","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-22DOI: 10.1016/j.tcb.2024.09.004
Jordan S Kesner, Xuebing Wu
The majority of the DNA sequence in our genome is noncoding and not intended for synthesizing proteins. Nonetheless, genome-wide mapping of ribosome footprints has revealed widespread translation in annotated noncoding sequences, including long noncoding RNAs (lncRNAs), untranslated regions (UTRs), and introns of mRNAs. How cells suppress the translation of potentially toxic proteins from various noncoding sequences remains poorly understood. This review summarizes mechanisms for the mitigation of noncoding translation, including the BCL2-associated athanogene 6 (BAG6)-mediated proteasomal degradation pathway, which has emerged as a unifying mechanism to suppress the translation of diverse noncoding sequences in metazoan cells.
{"title":"Mechanisms suppressing noncoding translation.","authors":"Jordan S Kesner, Xuebing Wu","doi":"10.1016/j.tcb.2024.09.004","DOIUrl":"https://doi.org/10.1016/j.tcb.2024.09.004","url":null,"abstract":"<p><p>The majority of the DNA sequence in our genome is noncoding and not intended for synthesizing proteins. Nonetheless, genome-wide mapping of ribosome footprints has revealed widespread translation in annotated noncoding sequences, including long noncoding RNAs (lncRNAs), untranslated regions (UTRs), and introns of mRNAs. How cells suppress the translation of potentially toxic proteins from various noncoding sequences remains poorly understood. This review summarizes mechanisms for the mitigation of noncoding translation, including the BCL2-associated athanogene 6 (BAG6)-mediated proteasomal degradation pathway, which has emerged as a unifying mechanism to suppress the translation of diverse noncoding sequences in metazoan cells.</p>","PeriodicalId":56085,"journal":{"name":"Trends in Cell Biology","volume":null,"pages":null},"PeriodicalIF":13.0,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142513570","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-21DOI: 10.1016/j.tcb.2024.09.005
Bo Shi, Thanh Kha Phan, Ivan K H Poon
Communication between dying and neighbouring cells is vital to ensure appropriate processes such as tissue repair or inflammation are initiated in response to cell death. As a mechanism to aid intercellular communication, cells undergoing apoptosis can release membrane-bound extracellular vesicles (EVs) called apoptotic-cell-derived EVs (ApoEVs) that can influence downstream processes through biomolecules within or on ApoEVs. ApoEVs are broadly categorised based on size as either large ApoEVs known as apoptotic bodies (ApoBDs) or small ApoEVs (s-ApoEVs). Notably, the mechanisms of ApoBD and s-ApoEV formation are different, and the functions of these two ApoEV subsets are distinct. This Review focuses on the biogenesis and functional properties of both ApoBDs and s-ApoEVs, particularly in the context of cell clearance, cell signalling and disease progression.
{"title":"Extracellular vesicles from the dead: the final message.","authors":"Bo Shi, Thanh Kha Phan, Ivan K H Poon","doi":"10.1016/j.tcb.2024.09.005","DOIUrl":"https://doi.org/10.1016/j.tcb.2024.09.005","url":null,"abstract":"<p><p>Communication between dying and neighbouring cells is vital to ensure appropriate processes such as tissue repair or inflammation are initiated in response to cell death. As a mechanism to aid intercellular communication, cells undergoing apoptosis can release membrane-bound extracellular vesicles (EVs) called apoptotic-cell-derived EVs (ApoEVs) that can influence downstream processes through biomolecules within or on ApoEVs. ApoEVs are broadly categorised based on size as either large ApoEVs known as apoptotic bodies (ApoBDs) or small ApoEVs (s-ApoEVs). Notably, the mechanisms of ApoBD and s-ApoEV formation are different, and the functions of these two ApoEV subsets are distinct. This Review focuses on the biogenesis and functional properties of both ApoBDs and s-ApoEVs, particularly in the context of cell clearance, cell signalling and disease progression.</p>","PeriodicalId":56085,"journal":{"name":"Trends in Cell Biology","volume":null,"pages":null},"PeriodicalIF":13.0,"publicationDate":"2024-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142513569","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}