Amelia W Paine, Rees F Garmann, Vinothan N Manoharan
{"title":"噬菌体MS2的细胞外剥离。","authors":"Amelia W Paine, Rees F Garmann, Vinothan N Manoharan","doi":"10.1016/j.jmb.2025.169316","DOIUrl":null,"url":null,"abstract":"<p><p>In the early stages of infection of its host, Escherichia coli, bacteriophage MS2 sheds its icosahedral protein capsid, after which the single-stranded genomic RNA (gRNA) and maturation protein enter the cell as a complex. Although the steps preceding uncoating, which include the binding of the Mat protein to the extracellular filament F-pilus, have been studied in detail, the uncoating step is not well understood. To study when and where uncoating happens, we image the infection process using fluorescence microscopy, separately labelling the MS2 capsid, its gRNA, and the cells. We do two types of experiments. In the first, we incubate the phage in a nonspecific intercalating dye, and we count the number of uncoated and intact phages before and after adding the labeled phages to cells. In the second, we examine the time course of infection by fixing unlabeled samples at different times after adding the phage, and then we label the MS2 gRNA using amplified fluorescence in situ hybridization. In both cases, we find that uncoating can occur anywhere on the F-pili, and that MS2 usually uncoats at a distance from the cell rather than at the cell surface. While these results do not rule out a current hypothesis that virus particles uncoat when the F-pilus retracts and brings them into contact with the cell body, they demonstrate an alternative, extracellular uncoating pathway. We discuss the possiblity that MS2 may have multiple uncoating pathways, and that the rate of each pathway could reflect a trade-off between different risk factors.</p>","PeriodicalId":369,"journal":{"name":"Journal of Molecular Biology","volume":" ","pages":"169316"},"PeriodicalIF":4.7000,"publicationDate":"2025-07-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Extracellular uncoating of bacteriophage MS2.\",\"authors\":\"Amelia W Paine, Rees F Garmann, Vinothan N Manoharan\",\"doi\":\"10.1016/j.jmb.2025.169316\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>In the early stages of infection of its host, Escherichia coli, bacteriophage MS2 sheds its icosahedral protein capsid, after which the single-stranded genomic RNA (gRNA) and maturation protein enter the cell as a complex. Although the steps preceding uncoating, which include the binding of the Mat protein to the extracellular filament F-pilus, have been studied in detail, the uncoating step is not well understood. To study when and where uncoating happens, we image the infection process using fluorescence microscopy, separately labelling the MS2 capsid, its gRNA, and the cells. We do two types of experiments. In the first, we incubate the phage in a nonspecific intercalating dye, and we count the number of uncoated and intact phages before and after adding the labeled phages to cells. In the second, we examine the time course of infection by fixing unlabeled samples at different times after adding the phage, and then we label the MS2 gRNA using amplified fluorescence in situ hybridization. In both cases, we find that uncoating can occur anywhere on the F-pili, and that MS2 usually uncoats at a distance from the cell rather than at the cell surface. While these results do not rule out a current hypothesis that virus particles uncoat when the F-pilus retracts and brings them into contact with the cell body, they demonstrate an alternative, extracellular uncoating pathway. We discuss the possiblity that MS2 may have multiple uncoating pathways, and that the rate of each pathway could reflect a trade-off between different risk factors.</p>\",\"PeriodicalId\":369,\"journal\":{\"name\":\"Journal of Molecular Biology\",\"volume\":\" \",\"pages\":\"169316\"},\"PeriodicalIF\":4.7000,\"publicationDate\":\"2025-07-03\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Journal of Molecular Biology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1016/j.jmb.2025.169316\",\"RegionNum\":2,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"BIOCHEMISTRY & MOLECULAR BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Molecular Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1016/j.jmb.2025.169316","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
In the early stages of infection of its host, Escherichia coli, bacteriophage MS2 sheds its icosahedral protein capsid, after which the single-stranded genomic RNA (gRNA) and maturation protein enter the cell as a complex. Although the steps preceding uncoating, which include the binding of the Mat protein to the extracellular filament F-pilus, have been studied in detail, the uncoating step is not well understood. To study when and where uncoating happens, we image the infection process using fluorescence microscopy, separately labelling the MS2 capsid, its gRNA, and the cells. We do two types of experiments. In the first, we incubate the phage in a nonspecific intercalating dye, and we count the number of uncoated and intact phages before and after adding the labeled phages to cells. In the second, we examine the time course of infection by fixing unlabeled samples at different times after adding the phage, and then we label the MS2 gRNA using amplified fluorescence in situ hybridization. In both cases, we find that uncoating can occur anywhere on the F-pili, and that MS2 usually uncoats at a distance from the cell rather than at the cell surface. While these results do not rule out a current hypothesis that virus particles uncoat when the F-pilus retracts and brings them into contact with the cell body, they demonstrate an alternative, extracellular uncoating pathway. We discuss the possiblity that MS2 may have multiple uncoating pathways, and that the rate of each pathway could reflect a trade-off between different risk factors.
期刊介绍:
Journal of Molecular Biology (JMB) provides high quality, comprehensive and broad coverage in all areas of molecular biology. The journal publishes original scientific research papers that provide mechanistic and functional insights and report a significant advance to the field. The journal encourages the submission of multidisciplinary studies that use complementary experimental and computational approaches to address challenging biological questions.
Research areas include but are not limited to: Biomolecular interactions, signaling networks, systems biology; Cell cycle, cell growth, cell differentiation; Cell death, autophagy; Cell signaling and regulation; Chemical biology; Computational biology, in combination with experimental studies; DNA replication, repair, and recombination; Development, regenerative biology, mechanistic and functional studies of stem cells; Epigenetics, chromatin structure and function; Gene expression; Membrane processes, cell surface proteins and cell-cell interactions; Methodological advances, both experimental and theoretical, including databases; Microbiology, virology, and interactions with the host or environment; Microbiota mechanistic and functional studies; Nuclear organization; Post-translational modifications, proteomics; Processing and function of biologically important macromolecules and complexes; Molecular basis of disease; RNA processing, structure and functions of non-coding RNAs, transcription; Sorting, spatiotemporal organization, trafficking; Structural biology; Synthetic biology; Translation, protein folding, chaperones, protein degradation and quality control.