Controlling the material properties and rRNA processing function of the nucleolus using light
The nucleolus is a prominent nuclear condensate that plays a central role in ribosome biogenesis by facilitating the transcription and processing of nascent ribosomal RNA (rRNA). A number of studies have highlighted the active viscoelastic nature of the nucleolus, whose material properties and phase...
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Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2019-08, Vol.116 (35), p.17330-17335 |
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description | The nucleolus is a prominent nuclear condensate that plays a central role in ribosome biogenesis by facilitating the transcription and processing of nascent ribosomal RNA (rRNA). A number of studies have highlighted the active viscoelastic nature of the nucleolus, whose material properties and phase behavior are a consequence of underlying molecular interactions. However, the ways in which the material properties of the nucleolus impact its function in rRNA biogenesis are not understood. Here we utilize the Cry2olig optogenetic system to modulate the viscoelastic properties of the nucleolus. We show that above a threshold concentration of Cry2olig protein, the nucleolus can be gelled into a tightly linked, low mobility meshwork. Gelled nucleoli no longer coalesce and relax into spheres but nonetheless permit continued internal molecular mobility of small proteins. These changes in nucleolar material properties manifest in specific alterations in rRNA processing steps, including a buildup of larger rRNA precursors and a depletion of smaller rRNA precursors. We propose that the flux of processed rRNA may be actively tuned by the cell through modulating nucleolar material properties, which suggests the potential of materials-based approaches for therapeutic intervention in ribosomopathies. |
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J. ; Brangwynne, Clifford P.</creator><creatorcontrib>Zhu, Lian ; Richardson, Tiffany M. ; Wacheul, Ludivine ; Wei, Ming-Tzo ; Feric, Marina ; Whitney, Gena ; Lafontaine, Denis L. J. ; Brangwynne, Clifford P.</creatorcontrib><description>The nucleolus is a prominent nuclear condensate that plays a central role in ribosome biogenesis by facilitating the transcription and processing of nascent ribosomal RNA (rRNA). A number of studies have highlighted the active viscoelastic nature of the nucleolus, whose material properties and phase behavior are a consequence of underlying molecular interactions. However, the ways in which the material properties of the nucleolus impact its function in rRNA biogenesis are not understood. Here we utilize the Cry2olig optogenetic system to modulate the viscoelastic properties of the nucleolus. We show that above a threshold concentration of Cry2olig protein, the nucleolus can be gelled into a tightly linked, low mobility meshwork. Gelled nucleoli no longer coalesce and relax into spheres but nonetheless permit continued internal molecular mobility of small proteins. These changes in nucleolar material properties manifest in specific alterations in rRNA processing steps, including a buildup of larger rRNA precursors and a depletion of smaller rRNA precursors. We propose that the flux of processed rRNA may be actively tuned by the cell through modulating nucleolar material properties, which suggests the potential of materials-based approaches for therapeutic intervention in ribosomopathies.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1903870116</identifier><identifier>PMID: 31399547</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; Biological Sciences ; Biosynthesis ; Cell Nucleolus - metabolism ; Coalescing ; Depletion ; Material properties ; Mice ; Mobility ; Molecular interactions ; NIH 3T3 Cells ; Nucleoli ; Optogenetics ; Precursors ; Proteins ; RNA processing ; RNA Processing, Post-Transcriptional - physiology ; RNA, Ribosomal - metabolism ; rRNA ; Transcription ; Viscoelasticity ; Xenopus laevis</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2019-08, Vol.116 (35), p.17330-17335</ispartof><rights>Copyright National Academy of Sciences Aug 27, 2019</rights><rights>2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c509t-b5217f5172130868b45b2d7072f1856685c3ff23ed25511ee11b09e8d0780a163</citedby><cites>FETCH-LOGICAL-c509t-b5217f5172130868b45b2d7072f1856685c3ff23ed25511ee11b09e8d0780a163</cites><orcidid>0000-0002-1350-9960 ; 0000-0001-7295-6288</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26850758$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26850758$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31399547$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhu, Lian</creatorcontrib><creatorcontrib>Richardson, Tiffany M.</creatorcontrib><creatorcontrib>Wacheul, Ludivine</creatorcontrib><creatorcontrib>Wei, Ming-Tzo</creatorcontrib><creatorcontrib>Feric, Marina</creatorcontrib><creatorcontrib>Whitney, Gena</creatorcontrib><creatorcontrib>Lafontaine, Denis L. J.</creatorcontrib><creatorcontrib>Brangwynne, Clifford P.</creatorcontrib><title>Controlling the material properties and rRNA processing function of the nucleolus using light</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The nucleolus is a prominent nuclear condensate that plays a central role in ribosome biogenesis by facilitating the transcription and processing of nascent ribosomal RNA (rRNA). A number of studies have highlighted the active viscoelastic nature of the nucleolus, whose material properties and phase behavior are a consequence of underlying molecular interactions. However, the ways in which the material properties of the nucleolus impact its function in rRNA biogenesis are not understood. Here we utilize the Cry2olig optogenetic system to modulate the viscoelastic properties of the nucleolus. We show that above a threshold concentration of Cry2olig protein, the nucleolus can be gelled into a tightly linked, low mobility meshwork. Gelled nucleoli no longer coalesce and relax into spheres but nonetheless permit continued internal molecular mobility of small proteins. These changes in nucleolar material properties manifest in specific alterations in rRNA processing steps, including a buildup of larger rRNA precursors and a depletion of smaller rRNA precursors. We propose that the flux of processed rRNA may be actively tuned by the cell through modulating nucleolar material properties, which suggests the potential of materials-based approaches for therapeutic intervention in ribosomopathies.</description><subject>Animals</subject><subject>Biological Sciences</subject><subject>Biosynthesis</subject><subject>Cell Nucleolus - metabolism</subject><subject>Coalescing</subject><subject>Depletion</subject><subject>Material properties</subject><subject>Mice</subject><subject>Mobility</subject><subject>Molecular interactions</subject><subject>NIH 3T3 Cells</subject><subject>Nucleoli</subject><subject>Optogenetics</subject><subject>Precursors</subject><subject>Proteins</subject><subject>RNA processing</subject><subject>RNA Processing, Post-Transcriptional - physiology</subject><subject>RNA, Ribosomal - metabolism</subject><subject>rRNA</subject><subject>Transcription</subject><subject>Viscoelasticity</subject><subject>Xenopus laevis</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc2LFDEQxYMo7uzq2ZPS4MVL71YlnU5yEZZBV2FRED1KSHenZzJkkjbpXvC_N7Ozjh-nQN6vXurlEfIC4RJBsKspmHyJCpgUgNg-IisEhXXbKHhMVgBU1LKhzRk5z3kHAIpLeErOGDKleCNW5Ps6hjlF713YVPPWVnsz2-SMr6YUJ5tmZ3NlwlClL5-uD3e9zfnAjkvoZxdDFcf7ubD03ka_5Gq5173bbOdn5MlofLbPH84L8u39u6_rD_Xt55uP6-vbuueg5rrjFMXIUVBkIFvZNbyjgwBBR5S8bSXv2ThSZgfKOaK1iB0oKwcQEgy27IK8PfpOS7e3Q29LJuP1lNzepJ86Gqf_VYLb6k28060ojwooBm8eDFL8sdg8673LvfXeBBuXrCkVKBvV8Kagr_9Dd3FJocQrlGSMlZVVoa6OVJ9izsmOp2UQ9KE6fahO_6muTLz6O8OJ_91VAV4egV2eYzrptHwPCC7ZL6_Onwc</recordid><startdate>20190827</startdate><enddate>20190827</enddate><creator>Zhu, Lian</creator><creator>Richardson, Tiffany M.</creator><creator>Wacheul, Ludivine</creator><creator>Wei, Ming-Tzo</creator><creator>Feric, Marina</creator><creator>Whitney, Gena</creator><creator>Lafontaine, Denis L. 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However, the ways in which the material properties of the nucleolus impact its function in rRNA biogenesis are not understood. Here we utilize the Cry2olig optogenetic system to modulate the viscoelastic properties of the nucleolus. We show that above a threshold concentration of Cry2olig protein, the nucleolus can be gelled into a tightly linked, low mobility meshwork. Gelled nucleoli no longer coalesce and relax into spheres but nonetheless permit continued internal molecular mobility of small proteins. These changes in nucleolar material properties manifest in specific alterations in rRNA processing steps, including a buildup of larger rRNA precursors and a depletion of smaller rRNA precursors. 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subjects | Animals Biological Sciences Biosynthesis Cell Nucleolus - metabolism Coalescing Depletion Material properties Mice Mobility Molecular interactions NIH 3T3 Cells Nucleoli Optogenetics Precursors Proteins RNA processing RNA Processing, Post-Transcriptional - physiology RNA, Ribosomal - metabolism rRNA Transcription Viscoelasticity Xenopus laevis |
title | Controlling the material properties and rRNA processing function of the nucleolus using light |
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